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| Publications of Susan C. Alberts :chronological alphabetical combined listing:%% Papers Published @article{fds376231, Author = {Anderson, JA and Lin, D and Lea, AJ and Johnston, RA and Voyles, T and Akinyi, MY and Archie, EA and Alberts, SC and Tung, J}, Title = {DNA methylation signatures of early-life adversity are exposure-dependent in wild baboons.}, Journal = {Proceedings of the National Academy of Sciences of the United States of America}, Volume = {121}, Number = {11}, Pages = {e2309469121}, Publisher = {Proceedings of the National Academy of Sciences}, Year = {2024}, Month = {March}, url = {http://dx.doi.org/10.1073/pnas.2309469121}, Abstract = {The early-life environment can profoundly shape the trajectory of an animal's life, even years or decades later. One mechanism proposed to contribute to these early-life effects is DNA methylation. However, the frequency and functional importance of DNA methylation in shaping early-life effects on adult outcomes is poorly understood, especially in natural populations. Here, we integrate prospectively collected data on fitness-associated variation in the early environment with DNA methylation estimates at 477,270 CpG sites in 256 wild baboons. We find highly heterogeneous relationships between the early-life environment and DNA methylation in adulthood: aspects of the environment linked to resource limitation (e.g., low-quality habitat, early-life drought) are associated with many more CpG sites than other types of environmental stressors (e.g., low maternal social status). Sites associated with early resource limitation are enriched in gene bodies and putative enhancers, suggesting they are functionally relevant. Indeed, by deploying a baboon-specific, massively parallel reporter assay, we show that a subset of windows containing these sites are capable of regulatory activity, and that, for 88% of early drought-associated sites in these regulatory windows, enhancer activity is DNA methylation-dependent. Together, our results support the idea that DNA methylation patterns contain a persistent signature of the early-life environment. However, they also indicate that not all environmental exposures leave an equivalent mark and suggest that socioenvironmental variation at the time of sampling is more likely to be functionally important. Thus, multiple mechanisms must converge to explain early-life effects on fitness-related traits.}, Doi = {10.1073/pnas.2309469121}, Key = {fds376231} } @article{fds372757, Author = {Levy, EJ and Lee, A and Long'ida Siodi and I and Helmich, EC and McLean, EM and Malone, EJ and Pickard, MJ and Ranjithkumar, R and Tung, J and Archie, EA and Alberts, SC}, Title = {Early life drought predicts components of adult body size in wild female baboons.}, Journal = {American journal of biological anthropology}, Volume = {182}, Number = {3}, Pages = {357-371}, Year = {2023}, Month = {November}, url = {http://dx.doi.org/10.1002/ajpa.24849}, Abstract = {<h4>Objectives</h4>In many taxa, adverse early-life environments are associated with reduced growth and smaller body size in adulthood. However, in wild primates, we know very little about whether, where, and to what degree trajectories are influenced by early adversity, or which types of early adversity matter most. Here, we use parallel-laser photogrammetry to assess inter-individual predictors of three measures of body size (leg length, forearm length, and shoulder-rump length) in a population of wild female baboons studied since birth.<h4>Materials and methods</h4>Using >2000 photogrammetric measurements of 127 females, we present a cross-sectional growth curve of wild female baboons (Papio cynocephalus) from juvenescence through adulthood. We then test whether females exposed to several important sources of early-life adversity-drought, maternal loss, low maternal rank, or a cumulative measure of adversity-were smaller for their age than females who experienced less adversity. Using the "animal model," we also test whether body size is heritable in this study population.<h4>Results</h4>Prolonged early-life drought predicted shorter limbs but not shorter torsos (i.e., shoulder-rump lengths). Our other measures of early-life adversity did not predict variation in body size. Heritability estimates for body size measures were 36%-67%. Maternal effects accounted for 13%-17% of the variance in leg and forearm length, but no variance in torso length.<h4>Discussion</h4>Our results suggest that baboon limbs, but not torsos, grow plastically in response to maternal effects and energetic early-life stress. Our results also reveal considerable heritability for all three body size measures in this study population.}, Doi = {10.1002/ajpa.24849}, Key = {fds372757} } @article{fds374187, Author = {Lange, EC and Griffin, M and Fogel, AS and Archie, EA and Tung, J and Alberts, SC}, Title = {Environmental, sex-specific and genetic determinants of infant social behaviour in a wild primate.}, Journal = {Proceedings. Biological sciences}, Volume = {290}, Number = {2011}, Pages = {20231597}, Year = {2023}, Month = {November}, url = {http://dx.doi.org/10.1098/rspb.2023.1597}, Abstract = {Affiliative social bonds are linked to fitness components in many social mammals. However, despite their importance, little is known about how the tendency to form social bonds develops in young animals, or if the timing of development is heritable and thus can evolve. Using four decades of longitudinal observational data from a wild baboon population, we assessed the environmental determinants of an important social developmental milestone in baboons-the age at which a young animal first grooms a conspecific-and we assessed how the rates at which offspring groom their mothers develops during the juvenile period. We found that grooming development differs between the sexes: female infants groom at an earlier age and reach equal rates of grooming with their mother earlier than males. We also found that age at first grooming for both sexes is weakly heritable (<i>h</i><sup>2</sup> = 0.043, 95% CI: 0.002-0.110). These results show that sex differences in grooming emerge at a young age; that strong, equitable social relationships between mothers and daughters begin very early in life; and that age at first grooming is heritable and therefore can be shaped by natural selection.}, Doi = {10.1098/rspb.2023.1597}, Key = {fds374187} } @article{fds371574, Author = {Tung, J and Lange, EC and Alberts, SC and Archie, EA}, Title = {Social and early life determinants of survival from cradle to grave: A case study in wild baboons.}, Journal = {Neuroscience and biobehavioral reviews}, Volume = {152}, Pages = {105282}, Year = {2023}, Month = {September}, url = {http://dx.doi.org/10.1016/j.neubiorev.2023.105282}, Abstract = {Field studies of natural mammal populations present powerful opportunities to investigate the determinants of health and aging using fine-grained observations of known individuals across the life course. Here, we synthesize five decades of findings from one such study: the wild baboons of the Amboseli ecosystem in Kenya. First, we discuss the profound associations between early life adversity, adult social conditions, and key aging outcomes in this population, especially survival. Second, we review potential mediators of the relationship between early life adversity and survival in our population. Notably, our tests of two leading candidate mediators-social isolation and glucocorticoid levels-fail to identify a single, strong mediator of early life effects on adult survival. Instead, early adversity, social isolation, and glucocorticoids are independently linked to adult lifespans, suggesting considerable scope for mitigating the negative consequences of early life adversity. Third, we review our work on the evolutionary rationale for early life effects on mortality, which currently argues against clear predictive adaptive responses. Finally, we end by highlighting major themes emerging from the study of sociality, development, and aging in the Amboseli baboons, as well as important open questions for future work.}, Doi = {10.1016/j.neubiorev.2023.105282}, Key = {fds371574} } @article{fds371102, Author = {Anderson, JA and Lin, D and Lea, AJ and Johnston, RA and Voyles, T and Akinyi, MY and Archie, EA and Alberts, SC and Tung, J}, Title = {DNA methylation signatures of early life adversity are exposure-dependent in wild baboons.}, Booktitle = {Cold Spring Harbor Laboratory}, Year = {2023}, Month = {June}, url = {http://dx.doi.org/10.1101/2023.06.05.542485}, Doi = {10.1101/2023.06.05.542485}, Key = {fds371102} } @article{fds362962, Author = {Zeng, S and Lange, EC and Archie, EA and Campos, FA and Alberts, SC and Li, F}, Title = {A Causal Mediation Model for Longitudinal Mediators and Survival Outcomes with an Application to Animal Behavior.}, Journal = {Journal of agricultural, biological, and environmental statistics}, Volume = {28}, Number = {2}, Pages = {197-218}, Year = {2023}, Month = {June}, url = {http://dx.doi.org/10.1007/s13253-022-00490-6}, Abstract = {In animal behavior studies, a common goal is to investigate the causal pathways between an exposure and outcome, and a mediator that lies in between. Causal mediation analysis provides a principled approach for such studies. Although many applications involve longitudinal data, the existing causal mediation models are not directly applicable to settings where the mediators are measured on irregular time grids. In this paper, we propose a causal mediation model that accommodates longitudinal mediators on arbitrary time grids and survival outcomes simultaneously. We take a functional data analysis perspective and view longitudinal mediators as realizations of underlying smooth stochastic processes. We define causal estimands of direct and indirect effects accordingly and provide corresponding identification assumptions. We employ a functional principal component analysis approach to estimate the mediator process and propose a Cox hazard model for the survival outcome that flexibly adjusts the mediator process. We then derive a g-computation formula to express the causal estimands using the model coefficients. The proposed method is applied to a longitudinal data set from the Amboseli Baboon Research Project to investigate the causal relationships between early adversity, adult physiological stress responses, and survival among wild female baboons. We find that adversity experienced in early life has a significant direct effect on females' life expectancy and survival probability, but find little evidence that these effects were mediated by markers of the stress response in adulthood. We further developed a sensitivity analysis method to assess the impact of potential violation to the key assumption of sequential ignorability. Supplementary materials accompanying this paper appear on-line.}, Doi = {10.1007/s13253-022-00490-6}, Key = {fds362962} } @article{fds370846, Author = {Lange, EC and Zeng, S and Campos, FA and Li, F and Tung, J and Archie, EA and Alberts, SC}, Title = {Early life adversity and adult social relationships have independent effects on survival in a wild primate.}, Journal = {Science advances}, Volume = {9}, Number = {20}, Pages = {eade7172}, Year = {2023}, Month = {May}, url = {http://dx.doi.org/10.1126/sciadv.ade7172}, Abstract = {Adverse conditions in early life can have negative consequences for adult health and survival in humans and other animals. What variables mediate the relationship between early adversity and adult survival? Adult social environments represent one candidate: Early life adversity is linked to social adversity in adulthood, and social adversity in adulthood predicts survival outcomes. However, no study has prospectively linked early life adversity, adult social behavior, and adult survival to measure the extent to which adult social behavior mediates this relationship. We do so in a wild baboon population in Amboseli, Kenya. We find weak mediation and largely independent effects of early adversity and adult sociality on survival. Furthermore, strong social bonds and high social status in adulthood can buffer some negative effects of early adversity. These results support the idea that affiliative social behavior is subject to natural selection through its positive relationship with survival, and they highlight possible targets for intervention to improve human health and well-being.}, Doi = {10.1126/sciadv.ade7172}, Key = {fds370846} } @article{fds367586, Author = {Sheldon, BC and Kruuk, LEB and Alberts, SC}, Title = {The expanding value of long-term studies of individuals in the wild.}, Journal = {Nature ecology & evolution}, Volume = {6}, Number = {12}, Pages = {1799-1801}, Publisher = {Springer Science and Business Media LLC}, Year = {2022}, Month = {December}, url = {http://dx.doi.org/10.1038/s41559-022-01940-7}, Doi = {10.1038/s41559-022-01940-7}, Key = {fds367586} } @article{fds366647, Author = {Ellis, S and Johnstone, RA and Cant, MA and Franks, DW and Weiss, MN and Alberts, SC and Balcomb, KC and Benton, CH and Brent, LJN and Crockford, C and Davidian, E and Delahay, RJ and Ellifrit, DK and Höner, OP and Meniri, M and McDonald, RA and Nichols, HJ and Thompson, FJ and Vigilant, L and Wittig, RM and Croft, DP}, Title = {Patterns and consequences of age-linked change in local relatedness in animal societies.}, Journal = {Nature ecology & evolution}, Volume = {6}, Number = {11}, Pages = {1766-1776}, Publisher = {Springer Science and Business Media LLC}, Year = {2022}, Month = {November}, url = {http://dx.doi.org/10.1038/s41559-022-01872-2}, Abstract = {The ultimate payoff of behaviours depends not only on their direct impact on an individual, but also on the impact on their relatives. Local relatedness-the average relatedness of an individual to their social environment-therefore has profound effects on social and life history evolution. Recent work has begun to show that local relatedness has the potential to change systematically over an individual's lifetime, a process called kinship dynamics. However, it is unclear how general these kinship dynamics are, whether they are predictable in real systems and their effects on behaviour and life history evolution. In this study, we combine modelling with data from real systems to explore the extent and impact of kinship dynamics. We use data from seven group-living mammals with diverse social and mating systems to demonstrate not only that kinship dynamics occur in animal systems, but also that the direction and magnitude of kinship dynamics can be accurately predicted using a simple model. We use a theoretical model to demonstrate that kinship dynamics can profoundly affect lifetime patterns of behaviour and can drive sex differences in helping and harming behaviour across the lifespan in social species. Taken together, this work demonstrates that kinship dynamics are likely to be a fundamental dimension of social evolution, especially when considering age-linked changes and sex differences in behaviour and life history.}, Doi = {10.1038/s41559-022-01872-2}, Key = {fds366647} } @article{fds367246, Author = {Paietta, EN and Weibel, CJ and Jansen, DA and Mututua, RS and Warutere, JK and Long'ida Siodi and I and Gesquiere, LR and Obanda, V and Alberts, SC and Archie, EA}, Title = {Troubled waters: Water availability drives human-baboon encounters in a protected, semi-arid landscape}, Journal = {Biological Conservation}, Volume = {274}, Year = {2022}, Month = {October}, url = {http://dx.doi.org/10.1016/j.biocon.2022.109740}, Abstract = {Most animal habitats are affected by humans. While some species tolerate and even benefit from these changes, others suffer. Understanding when and how human-altered landscapes affect animal behavior, health, reproduction, and survival is essential to species management in a human-dominated world. Here we use 27 years of data on human-baboon encounters in a protected, semi-arid ecosystem in Kenya to: (i) identify spatial, environmental, and group-level predictors of baboon encounters with pastoralists; (ii) test whether human-built water sources alter baboon ranging patterns; and (iii) test if human encounters are linked to baboon survival, reproduction, and health. We find that the primary driver of human-baboon encounters is water availability. During dry periods, pastoralists migrate into baboon rangelands, leading to frequent human-baboon encounters, especially near water wells. Further, the baboons shift their ranges to encompass newly built wells and move away from abandoned, dried-up wells. Since 2006, a third of adult baboon deaths were linked to violent encounters with humans or their dogs. Human encounters were also linked to high infant mortality and parasite diversity in females (but this effect could not be disentangled from seasonal confounds). For wild baboons, life in protected, pastoralist conservancies presents a double-edged sword: human-built wells enable the baboons to access water during dry periods, but these wells lead to encounters with humans, which have become a common source of baboon mortality. Together, our results serve as a comprehensive case study of anthropogenic effects on wild primates, highlighting the complex interactions between humans and wildlife in protected areas.}, Doi = {10.1016/j.biocon.2022.109740}, Key = {fds367246} } @article{fds363713, Author = {Björk, JR and Dasari, MR and Roche, K and Grieneisen, L and Gould, TJ and Grenier, J-C and Yotova, V and Gottel, N and Jansen, D and Gesquiere, LR and Gordon, JB and Learn, NH and Wango, TL and Mututua, RS and Kinyua Warutere, J and Siodi, L and Mukherjee, S and Barreiro, LB and Alberts, SC and Gilbert, JA and Tung, J and Blekhman, R and Archie, EA}, Title = {Synchrony and idiosyncrasy in the gut microbiome of wild baboons.}, Journal = {Nature ecology & evolution}, Volume = {6}, Number = {7}, Pages = {955-964}, Year = {2022}, Month = {July}, url = {http://dx.doi.org/10.1038/s41559-022-01773-4}, Abstract = {Human gut microbial dynamics are highly individualized, making it challenging to link microbiota to health and to design universal microbiome therapies. This individuality is typically attributed to variation in host genetics, diets, environments and medications but it could also emerge from fundamental ecological forces that shape microbiota more generally. Here, we leverage extensive gut microbial time series from wild baboons-hosts who experience little interindividual dietary and environmental heterogeneity-to test whether gut microbial dynamics are synchronized across hosts or largely idiosyncratic. Despite their shared lifestyles, baboon microbiota were only weakly synchronized. The strongest synchrony occurred among baboons living in the same social group, probably because group members range over the same habitat and simultaneously encounter the same sources of food and water. However, this synchrony was modest compared to each host's personalized dynamics. In support, host-specific factors, especially host identity, explained, on average, more than three times the deviance in longitudinal dynamics compared to factors shared with social group members and ten times the deviance of factors shared across the host population. These results contribute to mounting evidence that highly idiosyncratic gut microbiomes are not an artefact of modern human environments and that synchronizing forces in the gut microbiome (for example, shared environments, diets and microbial dispersal) are not strong enough to overwhelm key drivers of microbiome personalization, such as host genetics, priority effects, horizontal gene transfer and functional redundancy.}, Doi = {10.1038/s41559-022-01773-4}, Key = {fds363713} } @article{fds362499, Author = {Richardson, JL and Levy, EJ and Ranjithkumar, R and Yang, H and Monson, E and Cronin, A and Galbany, J and Robbins, MM and Alberts, SC and Reeves, ME and McFarlin, SC}, Title = {Automated, high-throughput image calibration for parallel-laser photogrammetry}, Journal = {Mammalian Biology}, Volume = {102}, Number = {3}, Pages = {615-627}, Year = {2022}, Month = {June}, url = {http://dx.doi.org/10.1007/s42991-021-00174-7}, Abstract = {Parallel-laser photogrammetry is growing in popularity as a way to collect non-invasive body size data from wild mammals. Despite its many appeals, this method requires researchers to hand-measure (i) the pixel distance between the parallel laser spots (inter-laser distance) to produce a scale within the image, and (ii) the pixel distance between the study subject’s body landmarks (inter-landmark distance). This manual effort is time-consuming and introduces human error: a researcher measuring the same image twice will rarely return the same values both times (resulting in within-observer error), as is also the case when two researchers measure the same image (resulting in between-observer error). Here, we present two independent methods that automate the inter-laser distance measurement of parallel-laser photogrammetry images. One method uses machine learning and image processing techniques in Python, and the other uses image processing techniques in ImageJ. Both of these methods reduce labor and increase precision without sacrificing accuracy. We first introduce the workflow of the two methods. Then, using two parallel-laser datasets of wild mountain gorilla and wild savannah baboon images, we validate the precision of these two automated methods relative to manual measurements and to each other. We also estimate the reduction of variation in final body size estimates in centimeters when adopting these automated methods, as these methods have no human error. Finally, we highlight the strengths of each method, suggest best practices for adopting either of them, and propose future directions for the automation of parallel-laser photogrammetry data.}, Doi = {10.1007/s42991-021-00174-7}, Key = {fds362499} } @article{fds363305, Author = {Bonnet, T and Morrissey, MB and de Villemereuil, P and Alberts, SC and Arcese, P and Bailey, LD and Boutin, S and Brekke, P and Brent, LJN and Camenisch, G and Charmantier, A and Clutton-Brock, TH and Cockburn, A and Coltman, DW and Courtiol, A and Davidian, E and Evans, SR and Ewen, JG and Festa-Bianchet, M and de Franceschi, C and Gustafsson, L and Höner, OP and Houslay, TM and Keller, LF and Manser, M and McAdam, AG and McLean, E and Nietlisbach, P and Osmond, HL and Pemberton, JM and Postma, E and Reid, JM and Rutschmann, A and Santure, AW and Sheldon, BC and Slate, J and Teplitsky, C and Visser, ME and Wachter, B and Kruuk, LEB}, Title = {Genetic variance in fitness indicates rapid contemporary adaptive evolution in wild animals.}, Journal = {Science (New York, N.Y.)}, Volume = {376}, Number = {6596}, Pages = {1012-1016}, Year = {2022}, Month = {May}, url = {http://dx.doi.org/10.1126/science.abk0853}, Abstract = {The rate of adaptive evolution, the contribution of selection to genetic changes that increase mean fitness, is determined by the additive genetic variance in individual relative fitness. To date, there are few robust estimates of this parameter for natural populations, and it is therefore unclear whether adaptive evolution can play a meaningful role in short-term population dynamics. We developed and applied quantitative genetic methods to long-term datasets from 19 wild bird and mammal populations and found that, while estimates vary between populations, additive genetic variance in relative fitness is often substantial and, on average, twice that of previous estimates. We show that these rates of contemporary adaptive evolution can affect population dynamics and hence that natural selection has the potential to partly mitigate effects of current environmental change.}, Doi = {10.1126/science.abk0853}, Key = {fds363305} } @article{fds363168, Author = {Campos, FA and Altmann, J and Cords, M and Fedigan, LM and Lawler, R and Lonsdorf, EV and Stoinski, TS and Strier, KB and Bronikowski, AM and Pusey, AE and Alberts, SC}, Title = {Female reproductive aging in seven primate species: Patterns and consequences.}, Journal = {Proceedings of the National Academy of Sciences of the United States of America}, Volume = {119}, Number = {20}, Pages = {e2117669119}, Year = {2022}, Month = {May}, url = {http://dx.doi.org/10.1073/pnas.2117669119}, Abstract = {Age-related changes in fertility have increasingly been documented in wild animal populations: In many species the youngest and oldest reproducers are disadvantaged relative to prime adults. How do these effects evolve, and what explains their diversity across species? Tackling this question requires detailed data on patterns of age-related reproductive performance in multiple animal species. Here, we compare patterns and consequences of age-related changes in female reproductive performance in seven primate populations that have been subjects of long-term continuous study for 29 to 57 y. We document evidence of age effects on fertility and on offspring performance in most, but not all, of these primate species. Specifically, females of six species showed longer interbirth intervals in the oldest age classes, youngest age classes, or both, and the oldest females also showed relatively fewer completed interbirth intervals. In addition, five species showed markedly lower survival among offspring born to the oldest mothers, and two species showed reduced survival for offspring born to both the youngest and the oldest mothers. In contrast, we found mixed evidence that maternal age affects the age at which daughters first reproduce: Only in muriquis and to some extent in chimpanzees, the only two species with female-biased dispersal, did relatively young mothers produce daughters that tended to have earlier first reproduction. Our findings demonstrate shared patterns as well as contrasts in age-related changes in female fertility across species of nonhuman primates and highlight species-specific behavior and life-history patterns as possible explanations for species-level differences.}, Doi = {10.1073/pnas.2117669119}, Key = {fds363168} } @article{fds362338, Author = {Galezo, AA and Nolas, MA and Fogel, AS and Mututua, RS and Warutere, JK and Siodi, IL and Altmann, J and Archie, EA and Tung, J and Alberts, SC}, Title = {Mechanisms of inbreeding avoidance in a wild primate.}, Journal = {Current biology : CB}, Volume = {32}, Number = {7}, Pages = {1607-1615.e4}, Year = {2022}, Month = {April}, url = {http://dx.doi.org/10.1016/j.cub.2022.01.082}, Abstract = {Inbreeding often imposes net fitness costs,<sup>1-5</sup> leading to the expectation that animals will engage in inbreeding avoidance when the costs of doing so are not prohibitive.<sup>4-9</sup> However, one recent meta-analysis indicates that animals of many species do not avoid mating with kin in experimental settings,<sup>6</sup> and another reports that behavioral inbreeding avoidance generally evolves only when kin regularly encounter each other and inbreeding costs are high.<sup>9</sup> These results raise questions about the processes that separate kin, how these processes depend on kin class and context, and whether kin classes differ in how effectively they avoid inbreeding via mate choice-in turn, demanding detailed demographic and behavioral data within individual populations. Here, we address these questions in a wild mammal population, the baboons of the Amboseli ecosystem in Kenya. We find that death and dispersal are very effective at separating opposite-sex pairs of close adult kin. Nonetheless, adult kin pairs do sometimes co-reside, and we find strong evidence for inbreeding avoidance via mate choice in kin classes with relatedness ≥0.25. Notably, maternal kin avoid inbreeding more effectively than paternal kin despite having identical coefficients of relatedness, pointing to kin discrimination as a potential constraint on effective inbreeding avoidance. Overall, demographic and behavioral processes ensure that inbred offspring are rare in undisturbed social groups (1% of offspring). However, in an anthropogenically disturbed social group with reduced male dispersal, we find inbreeding rates 10× higher. Our study reinforces the importance of demographic and behavioral contexts for understanding the evolution of inbreeding avoidance.<sup>9</sup>.}, Doi = {10.1016/j.cub.2022.01.082}, Key = {fds362338} } @article{fds363106, Author = {Malani, A and Rosenbaum, S and Alberts, SC and Archie, E}, Title = {Seeing the Future: A Better Way to Model and Test for Adaptive Developmental Plasticity}, Journal = {University of Chicago, Becker Friedman Institute for Economics Working Paper}, Number = {2022}, Year = {2022}, Month = {March}, Key = {fds363106} } @article{fds361297, Author = {Anderson, JA and Lea, AJ and Voyles, TN and Akinyi, MY and Nyakundi, R and Ochola, L and Omondi, M and Nyundo, F and Zhang, Y and Campos, FA and Alberts, SC and Archie, EA and Tung, J}, Title = {Distinct gene regulatory signatures of dominance rank and social bond strength in wild baboons.}, Journal = {Philosophical transactions of the Royal Society of London. Series B, Biological sciences}, Volume = {377}, Number = {1845}, Pages = {20200441}, Year = {2022}, Month = {February}, url = {http://dx.doi.org/10.1098/rstb.2020.0441}, Abstract = {The social environment is a major determinant of morbidity, mortality and Darwinian fitness in social animals. Recent studies have begun to uncover the molecular processes associated with these relationships, but the degree to which they vary across different dimensions of the social environment remains unclear. Here, we draw on a long-term field study of wild baboons to compare the signatures of affiliative and competitive aspects of the social environment in white blood cell gene regulation, under both immune-stimulated and non-stimulated conditions. We find that the effects of dominance rank on gene expression are directionally opposite in males versus females, such that high-ranking males resemble low-ranking females, and vice versa. Among females, rank and social bond strength are both reflected in the activity of cellular metabolism and proliferation genes. However, while we observe pronounced rank-related differences in baseline immune gene activity, only bond strength predicts the fold-change response to immune (lipopolysaccharide) stimulation. Together, our results indicate that the directionality and magnitude of social effects on gene regulation depend on the aspect of the social environment under study. This heterogeneity may help explain why social environmental effects on health and longevity can also vary between measures. This article is part of the theme issue 'The centennial of the pecking order: current state and future prospects for the study of dominance hierarchies'.}, Doi = {10.1098/rstb.2020.0441}, Key = {fds361297} } @article{fds363107, Author = {Malani, A and Rosenbaum, S and Alberts, SC and Archie, E}, Title = {Seeing the Future: A Better Way to Model and Test for Adaptive Developmental Plasticity}, Booktitle = {bioRxiv}, Year = {2022}, Month = {February}, url = {http://dx.doi.org/10.1101/2022.02.10.479998}, Doi = {10.1101/2022.02.10.479998}, Key = {fds363107} } @article{fds366224, Author = {Malani, A and Archie, E and Rosenbaum, S}, Title = {Conceptual and analytical approaches for modeling the developmental origins of inequality}, Booktitle = {bioRxiv}, Year = {2022}, url = {http://dx.doi.org/10.1101/2022.02.10.479998}, Doi = {10.1101/2022.02.10.479998}, Key = {fds366224} } @article{fds365952, Author = {Roche, K and Björk, J and Dasari, M and Grieneisen, L and Jansen, D and Gould, T and Gesquiere, L and Barreiro, L and Alberts, S and Blekhman, R and Gilbert, J and Tung, J and Mukherjee, S and Archie, E}, Title = {Universal gut microbial relationships in the gut microbiome of wild baboons}, Volume = {12}, Pages = {e83152}, Booktitle = {bioRxiv}, Year = {2022}, url = {http://dx.doi.org/10.1101/2022.08.20.504530}, Abstract = {Ecological relationships between bacteria mediate the services that gut microbiomes provide to their hosts. Knowing the overall direction and strength of these relationships is essential to learn how ecology scales up to affect microbiome assembly, dynamics, and host health. However, whether bacterial relationships are generalizable across hosts or personalized to individual hosts is debated. Here, we apply a robust, multinomial logistic-normal modeling framework to extensive time series data (5534 samples from 56 baboon hosts over 13 years) to infer thousands of correlations in bacterial abundance in individual baboons and test the degree to which bacterial abundance correlations are 'universal'. We also compare these patterns to two human data sets. We find that, most bacterial correlations are weak, negative, and universal across hosts, such that shared correlation patterns dominate over host-specific correlations by almost twofold. Further, taxon pairs that had inconsistent correlation signs (either positive or negative) in different hosts always had weak correlations within hosts. From the host perspective, host pairs with the most similar bacterial correlation patterns also had similar microbiome taxonomic compositions and tended to be genetic relatives. Compared to humans, universality in baboons was similar to that in human infants, and stronger than one data set from human adults. Bacterial families that showed universal correlations in human infants were often universal in baboons. Together, our work contributes new tools for analyzing the universality of bacterial associations across hosts, with implications for microbiome personalization, community assembly, and stability, and for designing microbiome interventions to improve host health.}, Doi = {10.1101/2022.08.20.504530}, Key = {fds365952} } @article{fds366471, Author = {Lange, E and Zeng, S and Campos, F and Li, F and Tung, J and Archie, E and Alberts, S}, Title = {Early life adversity and adult social relationships have independent effects on survival in a wild animal model of aging}, Booktitle = {bioRxiv}, Year = {2022}, url = {http://dx.doi.org/10.1101/2022.09.06.506810}, Doi = {10.1101/2022.09.06.506810}, Key = {fds366471} } @article{fds366473, Author = {McLean, E and Moorad, J and Tung, J and Archie, E and Alberts, S}, Title = {Genetic variance and indirect genetic effects for affiliative social behavior in a wild primate}, Volume = {77}, Number = {7}, Pages = {1607-1621}, Booktitle = {bioRxiv}, Year = {2022}, url = {http://dx.doi.org/10.1101/2022.08.29.505695}, Abstract = {Affiliative social behaviors are linked to fitness components in multiple species. However, the role of genetic variance in shaping such behaviors remains largely unknown, limiting our understanding of how affiliative behaviors can respond to natural selection. Here, we employed the "animal model" to estimate environmental and genetic sources of variance and covariance in grooming behavior in the well-studied Amboseli wild baboon population. We found that the tendency for a female baboon to groom others ("grooming given") is heritable (h2 = 0.22 ± 0.048), and that several environmental variables-including dominance rank and the availability of kin as grooming partners-contribute to variance in this grooming behavior. We also detected small but measurable variance due to the indirect genetic effect of partner identity on the amount of grooming given within dyadic grooming partnerships. The indirect and direct genetic effects for grooming given were positively correlated (r = 0.74 ± 0.09). Our results provide insight into the evolvability of affiliative behavior in wild animals, including the possibility for correlations between direct and indirect genetic effects to accelerate the response to selection. As such they provide novel information about the genetic architecture of social behavior in nature, with important implications for the evolution of cooperation and reciprocity.}, Doi = {10.1101/2022.08.29.505695}, Key = {fds366473} } @article{fds367587, Author = {Lange, E and Griffin, M and Fogel, A and Archie, E and Tung, J and Alberts, S}, Title = {Heritable and sex-specific variation in the development of social behavior in a wild primate}, Booktitle = {bioRxiv}, Year = {2022}, url = {http://dx.doi.org/10.1101/2022.10.21.513189}, Doi = {10.1101/2022.10.21.513189}, Key = {fds367587} } @article{fds366472, Author = {Fogel, A and Oduor, P and Nyongesa, A and Kimwele, C and Alberts, S and Archie, E and Tung, J}, Title = {Ecology and age, but not genetic ancestry, predict fetal loss in a wild baboon hybrid zone}, Volume = {180}, Number = {4}, Pages = {618-632}, Booktitle = {bioRxiv}, Year = {2022}, url = {http://dx.doi.org/10.1101/2022.09.03.505836}, Abstract = {<h4>Objectives</h4>Pregnancy failure represents a major fitness cost for any mammal, particularly those with slow life histories such as primates. Here, we quantified the risk of fetal loss in wild hybrid baboons, including genetic, ecological, and demographic sources of variance. We were particularly interested in testing the hypothesis that hybridization increases fetal loss rates. Such an effect would help explain how baboons may maintain genetic and phenotypic integrity despite interspecific gene flow.<h4>Materials and methods</h4>We analyzed outcomes for 1020 pregnancies observed over 46 years in a natural yellow baboon-anubis baboon hybrid zone. Fetal losses and live births were scored based on records of female reproductive state and the appearance of live neonates. We modeled the probability of fetal loss as a function of a female's genetic ancestry (the proportion of her genome estimated to be descended from anubis [vs. yellow] ancestors), age, number of previous fetal losses, dominance rank, group size, climate, and habitat quality using binomial mixed effects models.<h4>Results</h4>Female genetic ancestry did not predict fetal loss. Instead, the risk of fetal loss is elevated for very young and very old females. Fetal loss is most robustly predicted by ecological factors, including poor habitat quality prior to a home range shift and extreme heat during pregnancy.<h4>Discussion</h4>Our results suggest that gene flow between yellow and anubis baboons is not impeded by an increased risk of fetal loss for hybrid females. Instead, ecological conditions and female age are key determinants of this component of female reproductive success.}, Doi = {10.1101/2022.09.03.505836}, Key = {fds366472} } @article{fds366474, Author = {Zipple, M and Archie, E and Tung, J and Mututua, R and Warutere, K and Siodi, L and Altmann, J and Alberts, S}, Title = {Five decades of data yield no support for adaptive biasing of offspring sex ratio in wild baboons (Papio cynocephalus)}, Volume = {202}, Number = {4}, Pages = {383-398}, Booktitle = {bioRxiv}, Publisher = {University of Chicago Press}, Year = {2022}, url = {http://dx.doi.org/10.1101/2022.08.28.505562}, Abstract = {AbstractOver the past 50 years, a wealth of testable, often conflicting hypotheses have been generated about the evolution of offspring sex ratio manipulation by mothers. Several of these hypotheses have received support in studies of invertebrates and some vertebrate taxa. However, their success in explaining sex ratios in mammalian taxa-especially in primates-has been mixed. Here, we assess the predictions of four different hypotheses about the evolution of biased offspring sex ratios in the baboons of the Amboseli basin in Kenya: the Trivers-Willard, female rank enhancement, local resource competition, and local resource enhancement hypotheses. Using the largest sample size ever analyzed in a primate population (n=1,372 offspring), we test the predictions of each hypothesis. Overall, we find no support for adaptive biasing of sex ratios. Offspring sex is not consistently related to maternal dominance rank or biased toward the dispersing sex, nor is it predicted by group size, population growth rates, or their interaction with maternal rank. Because our sample size confers power to detect even subtle biases in sex ratio, including modulation by environmental heterogeneity, these results suggest that adaptive biasing of offspring sex does not occur in this population.}, Doi = {10.1101/2022.08.28.505562}, Key = {fds366474} } @article{fds360543, Author = {Lerch, BA and Abbott, KC and Archie, EA and Alberts, SC}, Title = {Better baboon break-ups: collective decision theory of complex social network fissions.}, Journal = {Proceedings. Biological sciences}, Volume = {288}, Number = {1964}, Pages = {20212060}, Year = {2021}, Month = {December}, url = {http://dx.doi.org/10.1098/rspb.2021.2060}, Abstract = {Many social groups are made up of complex social networks in which each individual associates with a distinct subset of its groupmates. If social groups become larger over time, competition often leads to a permanent group fission. During such fissions, complex social networks present a collective decision problem and a multidimensional optimization problem: it is advantageous for each individual to remain with their closest allies after a fission, but impossible for every individual to do so. Here, we develop computational algorithms designed to simulate group fissions in a network-theoretic framework. We focus on three fission algorithms (democracy, community and despotism) that fall on a spectrum from a democratic to a dictatorial collective decision. We parameterize our social networks with data from wild baboons (<i>Papio cynocephalus</i>) and compare our simulated fissions with actual baboon fission events. We find that the democracy and community algorithms (egalitarian decisions where each individual influences the outcome) better maintain social networks during simulated fissions than despotic decisions (driven primarily by a single individual). We also find that egalitarian decisions are better at predicting the observed individual-level outcomes of observed fissions, although the observed fissions often disturbed their social networks more than the simulated egalitarian fissions.}, Doi = {10.1098/rspb.2021.2060}, Key = {fds360543} } @article{fds358806, Author = {Fogel, AS and McLean, EM and Gordon, JB and Archie, EA and Tung, J and Alberts, SC}, Title = {Genetic ancestry predicts male-female affiliation in a natural baboon hybrid zone.}, Journal = {Animal behaviour}, Volume = {180}, Pages = {249-268}, Publisher = {Elsevier BV}, Year = {2021}, Month = {October}, url = {http://dx.doi.org/10.1016/j.anbehav.2021.07.009}, Abstract = {Opposite-sex social relationships are important predictors of fitness in many animals, including several group-living mammals. Consequently, understanding sources of variance in the tendency to form opposite-sex relationships is important for understanding social evolution. Genetic contributions are of particular interest due to their importance in long-term evolutionary change, but little is known about genetic effects on male-female relationships in social mammals, especially outside of the mating context. Here, we investigate the effects of genetic ancestry on male-female affiliative behaviour in a hybrid zone between the yellow baboon, <i>Papio cynocephalus</i>, and the anubis baboon, <i>Papio anubis</i>, in a population in which male-female social bonds are known predictors of life span. We place our analysis within the context of other social and demographic predictors of affiliative behaviour in baboons. Genetic ancestry was the most consistent predictor of opposite-sex affiliative behaviour we observed, with the exception of strong effects of dominance rank. Our results show that increased anubis genetic ancestry is associated with a subtle, but significantly higher, probability of opposite-sex affiliative behaviour, in both males and females. Additionally, pairs of anubis-like males and anubis-like females were the most likely to socially affiliate, resulting in moderate assortativity in grooming and proximity behaviour as a function of genetic ancestry. Our findings indicate that opposite-sex affiliative behaviour partially diverged during baboon evolution to differentiate yellow and anubis baboons, despite overall similarities in their social structures and mating systems. Furthermore, they suggest that affiliative behaviour may simultaneously promote and constrain baboon admixture, through additive and assortative effects of ancestry, respectively.}, Doi = {10.1016/j.anbehav.2021.07.009}, Key = {fds358806} } @article{fds355661, Author = {Zipple, MN and Roberts, EK and Alberts, SC and Beehner, JC}, Title = {The Bruce effect should be defined by function, not mechanism: comments on ‘How to escape male infanticide: mechanisms for avoiding or terminating pregnancy in mammals’}, Journal = {Mammal Review}, Volume = {51}, Number = {4}, Pages = {596-599}, Year = {2021}, Month = {October}, url = {http://dx.doi.org/10.1111/mam.12250}, Abstract = {Bartoš et al. (2021; Mammal Review 51: 143–153; https://doi.org/10.1111/mam.12219) reviewed the mechanisms involved in the ‘Bruce effect’ – a phenomenon originally documented in inseminated female house mice Mus musculus, who block pregnancy following exposure to a novel (non-sire) male. They argue that the term ‘Bruce effect’ should be applied in cases that are mechanistically equivalent to this original observation in mice. We argue that the Bruce effect should be defined instead by its function: a phenomenon by which inseminated or pregnant females benefit by blocking or terminating pregnancy following exposure to a non-sire male. Only functional definitions of phenomena allow for the articulation and testing of evolutionary hypotheses.}, Doi = {10.1111/mam.12250}, Key = {fds355661} } @article{fds359021, Author = {Lea, AJ and Akinyi, MY and Nyakundi, R and Mareri, P and Nyundo, F and Kariuki, T and Alberts, SC and Archie, EA and Tung, J}, Title = {Erratum: Dominance rank-associated gene expression is widespread, sex-specific, and a precursor to high social status in wild male baboons (Proceedings of the National Academy of Sciences of the United States of America (2018) 115 (E12163–E12171) DOI: 10.1073/pnas.1811967115)}, Journal = {Proceedings of the National Academy of Sciences of the United States of America}, Volume = {118}, Number = {36}, Year = {2021}, Month = {September}, url = {http://dx.doi.org/10.1073/pnas.2114104118}, Abstract = {Correction to Supporting Information for “Dominance rank-associated gene expression is widespread, sex-specific, and a precursor to high social status in wild male baboons,” by Amanda J. Lea, Mercy Y. Akinyi, Ruth Nyakundi, Peter Mareri, Fred Nyundo, Thomas Kariuki, Susan C. Alberts, Elizabeth A. Archie, and Jenny Tung, which was first published December 11, 2018; 10.1073/pnas.1811967115 (Proc. Natl. Acad. Sci. U.S.A. 115, E12163–E12171). The authors note that, in the SI Appendix, the concentration of the lipopolysaccharide stimulant on page 3, first full paragraph, line 4 was reported incorrectly. Subsequently, “1 ug/mL lipopolysaccharide” should instead appear as “0.1 ug/mL lipopolysaccharide.” The SI Appendix has been corrected online.}, Doi = {10.1073/pnas.2114104118}, Key = {fds359021} } @article{fds357895, Author = {Grieneisen, L and Dasari, M and Gould, TJ and Björk, JR and Grenier, J-C and Yotova, V and Jansen, D and Gottel, N and Gordon, JB and Learn, NH and Gesquiere, LR and Wango, TL and Mututua, RS and Warutere, JK and Siodi, L and Gilbert, JA and Barreiro, LB and Alberts, SC and Tung, J and Archie, EA and Blekhman, R}, Title = {Gut microbiome heritability is nearly universal but environmentally contingent.}, Journal = {Science (New York, N.Y.)}, Volume = {373}, Number = {6551}, Pages = {181-186}, Year = {2021}, Month = {July}, url = {http://dx.doi.org/10.1126/science.aba5483}, Abstract = {Relatives have more similar gut microbiomes than nonrelatives, but the degree to which this similarity results from shared genotypes versus shared environments has been controversial. Here, we leveraged 16,234 gut microbiome profiles, collected over 14 years from 585 wild baboons, to reveal that host genetic effects on the gut microbiome are nearly universal. Controlling for diet, age, and socioecological variation, 97% of microbiome phenotypes were significantly heritable, including several reported as heritable in humans. Heritability was typically low (mean = 0.068) but was systematically greater in the dry season, with low diet diversity, and in older hosts. We show that longitudinal profiles and large sample sizes are crucial to quantifying microbiome heritability, and indicate scope for selection on microbiome characteristics as a host phenotype.}, Doi = {10.1126/science.aba5483}, Key = {fds357895} } @article{fds358287, Author = {Zeng, S and Rosenbaum, S and Alberts, SC and Archie, EA and Li, F}, Title = {Causal mediation analysis for sparse and irregular longitudinal data}, Journal = {Annals of Applied Statistics}, Volume = {15}, Number = {2}, Pages = {747-767}, Year = {2021}, Month = {June}, url = {http://dx.doi.org/10.1214/20-AOAS1427}, Abstract = {Causal mediation analysis seeks to investigate how the treatment effect of an exposure on outcomes is mediated through intermediate variables. Although many applications involve longitudinal data, the existing methods are not directly applicable to settings where the mediator and outcome are measured on sparse and irregular time grids. We extend the existing causal mediation framework from a functional data analysis perspective, viewing the sparse and irregular longitudinal data as realizations of underlying smooth stochastic processes. We define causal estimands of direct and indirect effects accordingly and provide corresponding identification assumptions. For estimation and inference, we employ a functional principal component analysis approach for dimension reduction and use the first few functional principal components instead of the whole trajectories in the structural equation models. We adopt the Bayesian paradigm to accurately quantify the uncertainties. The operating characteristics of the proposed methods are examined via simulations. We apply the proposed methods to a longitudinal data set from a wild baboon population in Kenya to investigate the causal relationships between early adversity, strength of social bonds between animals and adult glucocorticoid hormone concentrations. We find that early adversity has a significant direct effect (a 9-14% increase) on females’ glucocorticoid concentrations across adulthood but find little evidence that these effects were mediated by weak social bonds.}, Doi = {10.1214/20-AOAS1427}, Key = {fds358287} } @article{fds357290, Author = {Colchero, F and Aburto, JM and Archie, EA and Boesch, C and Breuer, T and Campos, FA and Collins, A and Conde, DA and Cords, M and Crockford, C and Thompson, ME and Fedigan, LM and Fichtel, C and Groenenberg, M and Hobaiter, C and Kappeler, PM and Lawler, RR and Lewis, RJ and Machanda, ZP and Manguette, ML and Muller, MN and Packer, C and Parnell, RJ and Perry, S and Pusey, AE and Robbins, MM and Seyfarth, RM and Silk, JB and Staerk, J and Stoinski, TS and Stokes, EJ and Strier, KB and Strum, SC and Tung, J and Villavicencio, F and Wittig, RM and Wrangham, RW and Zuberbühler, K and Vaupel, JW and Alberts, SC}, Title = {The long lives of primates and the 'invariant rate of ageing' hypothesis.}, Journal = {Nature communications}, Volume = {12}, Number = {1}, Pages = {3666}, Year = {2021}, Month = {June}, url = {http://dx.doi.org/10.1038/s41467-021-23894-3}, Abstract = {Is it possible to slow the rate of ageing, or do biological constraints limit its plasticity? We test the 'invariant rate of ageing' hypothesis, which posits that the rate of ageing is relatively fixed within species, with a collection of 39 human and nonhuman primate datasets across seven genera. We first recapitulate, in nonhuman primates, the highly regular relationship between life expectancy and lifespan equality seen in humans. We next demonstrate that variation in the rate of ageing within genera is orders of magnitude smaller than variation in pre-adult and age-independent mortality. Finally, we demonstrate that changes in the rate of ageing, but not other mortality parameters, produce striking, species-atypical changes in mortality patterns. Our results support the invariant rate of ageing hypothesis, implying biological constraints on how much the human rate of ageing can be slowed.}, Doi = {10.1038/s41467-021-23894-3}, Key = {fds357290} } @article{fds355776, Author = {Anderson, JA and Johnston, RA and Lea, AJ and Campos, FA and Voyles, TN and Akinyi, MY and Alberts, SC and Archie, EA and Tung, J}, Title = {High social status males experience accelerated epigenetic aging in wild baboons.}, Journal = {eLife}, Volume = {10}, Pages = {e66128}, Year = {2021}, Month = {April}, url = {http://dx.doi.org/10.7554/elife.66128}, Abstract = {Aging, for virtually all life, is inescapable. However, within populations, biological aging rates vary. Understanding sources of variation in this process is central to understanding the biodemography of natural populations. We constructed a DNA methylation-based age predictor for an intensively studied wild baboon population in Kenya. Consistent with findings in humans, the resulting 'epigenetic clock' closely tracks chronological age, but individuals are predicted to be somewhat older or younger than their known ages. Surprisingly, these deviations are not explained by the strongest predictors of lifespan in this population, early adversity and social integration. Instead, they are best predicted by male dominance rank: high-ranking males are predicted to be older than their true ages, and epigenetic age tracks changes in rank over time. Our results argue that achieving high rank for male baboons - the best predictor of reproductive success - imposes costs consistent with a 'live fast, die young' life-history strategy.}, Doi = {10.7554/elife.66128}, Key = {fds355776} } @article{fds355933, Author = {Campos, FA and Archie, EA and Gesquiere, LR and Tung, J and Altmann, J and Alberts, SC}, Title = {Glucocorticoid exposure predicts survival in female baboons.}, Journal = {Science advances}, Volume = {7}, Number = {17}, Pages = {eabf6759}, Year = {2021}, Month = {April}, url = {http://dx.doi.org/10.1126/sciadv.abf6759}, Abstract = {Are differences in hypothalamic-pituitary-adrenal (HPA) axis activation across the adult life span linked to differences in survival? This question has been the subject of considerable debate. We analyze the link between survival and fecal glucocorticoid (GC) measures in a wild primate population, leveraging an unusually extensive longitudinal dataset of 14,173 GC measurements from 242 adult female baboons over 1634 female years. We document a powerful link between GCs and survival: Females with relatively high current GCs or high lifelong cumulative GCs face an elevated risk of death. A hypothetical female who maintained GCs in the top 90% for her age across adulthood would be expected to lose 5.4 years of life relative to a female who maintained GCs in the bottom 10% for her age. Hence, differences among individuals in HPA axis activity provide valuable prognostic information about disparities in life span.}, Doi = {10.1126/sciadv.abf6759}, Key = {fds355933} } @article{fds354523, Author = {Zipple, MN and Altmann, J and Campos, FA and Cords, M and Fedigan, LM and Lawler, RR and Lonsdorf, EV and Perry, S and Pusey, AE and Stoinski, TS and Strier, KB and Alberts, SC}, Title = {Maternal death and offspring fitness in multiple wild primates.}, Journal = {Proceedings of the National Academy of Sciences of the United States of America}, Volume = {118}, Number = {1}, Pages = {e2015317118}, Year = {2021}, Month = {January}, url = {http://dx.doi.org/10.1073/pnas.2015317118}, Abstract = {Primate offspring often depend on their mothers well beyond the age of weaning, and offspring that experience maternal death in early life can suffer substantial reductions in fitness across the life span. Here, we leverage data from eight wild primate populations (seven species) to examine two underappreciated pathways linking early maternal death and offspring fitness that are distinct from direct effects of orphaning on offspring survival. First, we show that, for five of the seven species, offspring face reduced survival during the years immediately preceding maternal death, while the mother is still alive. Second, we identify an intergenerational effect of early maternal loss in three species (muriquis, baboons, and blue monkeys), such that early maternal death experienced in one generation leads to reduced offspring survival in the next. Our results have important implications for the evolution of slow life histories in primates, as they suggest that maternal condition and survival are more important for offspring fitness than previously realized.}, Doi = {10.1073/pnas.2015317118}, Key = {fds354523} } @article{fds363028, Author = {Vilgalys, T and Fogel, A and Mututua, R and Kinyua Warutere and J and Siodi, L and Anderson, J and Kim, SY and Voyles, T and Robinson, J and Wall, J and Archie, E and Alberts, S and Tung, J}, Title = {Selection against admixture and gene regulatory divergence in a long-term primate field study}, Volume = {377}, Number = {6606}, Pages = {635-641}, Year = {2021}, url = {http://dx.doi.org/10.1101/2021.08.19.456711}, Abstract = {Admixture has profoundly influenced evolution across the tree of life, including in humans and other primates 1,2 . However, we have limited insight into the genetic and phenotypic consequences of admixture in primates, especially during its key early stages. Here, we address this gap by combining 50 years of field observations with population and functional genomic data from yellow ( Papio cynocephalus ) and anubis ( P. anubis ) baboons in Kenya, in a longitudinally studied population that has experienced both historical and recent admixture 3 . We use whole-genome sequencing to characterize the extent of the hybrid zone, estimate local ancestry for 442 known individuals, and predict the landscape of introgression across the genome. Despite no major fitness costs to hybrids, we identify signatures of selection against introgression that are strikingly similar to those described for archaic hominins 4–6 . These signatures are strongest near loci with large ancestry effects on gene expression, supporting the importance of gene regulation in primate evolution and the idea that selection targeted large regulatory effects following archaic hominin admixture 7,8 . Our results show that genomic data and field observations of hybrids are important and mutually informative. They therefore demonstrate the value of other primates as living models for phenomena that we cannot observe in our own lineage.}, Doi = {10.1101/2021.08.19.456711}, Key = {fds363028} } @article{fds352369, Author = {Campos, FA and Villavicencio, F and Archie, EA and Colchero, F and Alberts, SC}, Title = {Social bonds, social status and survival in wild baboons: a tale of two sexes.}, Journal = {Philosophical transactions of the Royal Society of London. Series B, Biological sciences}, Volume = {375}, Number = {1811}, Pages = {20190621}, Year = {2020}, Month = {November}, url = {http://dx.doi.org/10.1098/rstb.2019.0621}, Abstract = {People who are more socially integrated or have higher socio-economic status live longer. Recent studies in non-human primates show striking convergences with this human pattern: female primates with more social partners, stronger social bonds or higher dominance rank all lead longer lives. However, it remains unclear whether social environments also predict survival in male non-human primates, as it does in men. This gap persists because, in most primates, males disperse among social groups, resulting in many males who disappear with unknown fate and have unknown dates of birth. We present a Bayesian model to estimate the effects of time-varying social covariates on age-specific adult mortality in both sexes of wild baboons. We compare how the survival trajectories of both sexes are linked to social bonds and social status over the life. We find that, parallel to females, male baboons who are more strongly bonded to females have longer lifespans. However, males with higher dominance rank for their age appear to have shorter lifespans. This finding brings new understanding to the adaptive significance of heterosexual social bonds for male baboons: in addition to protecting the male's offspring from infanticide, these bonds may have direct benefits to males themselves. This article is part of the theme issue 'Evolution of the primate ageing process'.}, Doi = {10.1098/rstb.2019.0621}, Key = {fds352369} } @article{fds352370, Author = {Weibel, CJ and Tung, J and Alberts, SC and Archie, EA}, Title = {Accelerated reproduction is not an adaptive response to early-life adversity in wild baboons.}, Journal = {Proceedings of the National Academy of Sciences of the United States of America}, Volume = {117}, Number = {40}, Pages = {24909-24919}, Year = {2020}, Month = {October}, url = {http://dx.doi.org/10.1073/pnas.2004018117}, Abstract = {In humans and other long-lived species, harsh conditions in early life often lead to profound differences in adult life expectancy. In response, natural selection is expected to accelerate the timing and pace of reproduction in individuals who experience some forms of early-life adversity. However, the adaptive benefits of reproductive acceleration following early adversity remain untested. Here, we test a recent version of this theory, the internal predictive adaptive response (iPAR) model, by assessing whether accelerating reproduction following early-life adversity leads to higher lifetime reproductive success. We do so by leveraging 48 y of continuous, individual-based data from wild female baboons in the Amboseli ecosystem in Kenya, including prospective, longitudinal data on multiple sources of nutritional and psychosocial adversity in early life; reproductive pace; and lifetime reproductive success. We find that while early-life adversity led to dramatically shorter lifespans, individuals who experienced early adversity did not accelerate their reproduction compared with those who did not experience early adversity. Further, while accelerated reproduction predicted increased lifetime reproductive success overall, these benefits were not specific to females who experienced early-life adversity. Instead, females only benefited from reproductive acceleration if they also led long lives. Our results call into question the theory that accelerated reproduction is an adaptive response to both nutritional and psychosocial sources of early-life adversity in baboons and other long-lived species.}, Doi = {10.1073/pnas.2004018117}, Key = {fds352370} } @article{fds351178, Author = {Levy, EJ and Gesquiere, LR and McLean, E and Franz, M and Warutere, JK and Sayialel, SN and Mututua, RS and Wango, TL and Oudu, VK and Altmann, J and Archie, EA and Alberts, SC}, Title = {Higher dominance rank is associated with lower glucocorticoids in wild female baboons: A rank metric comparison.}, Journal = {Hormones and behavior}, Volume = {125}, Pages = {104826}, Year = {2020}, Month = {September}, url = {http://dx.doi.org/10.1016/j.yhbeh.2020.104826}, Abstract = {In vertebrates, glucocorticoid secretion occurs in response to energetic and psychosocial stressors that trigger the hypothalamic-pituitary-adrenal (HPA) axis. Measuring glucocorticoid concentrations can therefore shed light on the stressors associated with different social and environmental variables, including dominance rank. Using 14,172 fecal samples from 237 wild female baboons, we test the hypothesis that high-ranking females experience fewer psychosocial and/or energetic stressors than lower-ranking females. We predicted that high-ranking females would have lower fecal glucocorticoid (fGC) concentrations than low-ranking females. Because dominance rank can be measured in multiple ways, we employ an information theoretic approach to compare 5 different measures of rank as predictors of fGC concentrations: ordinal rank; proportional rank; Elo rating; and two approaches to categorical ranking (alpha vs non-alpha and high-middle-low). Our hypothesis was supported, but it was also too simplistic. We found that alpha females exhibited substantially lower fGCs than other females (typical reduction = 8.2%). If we used proportional rank instead of alpha versus non-alpha status in the model, we observed a weak effect of rank such that fGCs rose 4.2% from the highest- to lowest-ranking female in the hierarchy. Models using ordinal rank, Elo rating, or high-middle-low categories alone failed to explain variation in female fGCs. Our findings shed new light on the association between dominance rank and the stress response, the competitive landscape of female baboons as compared to males, and the assumptions inherent in a researcher's choice of rank metric.}, Doi = {10.1016/j.yhbeh.2020.104826}, Key = {fds351178} } @article{fds352212, Author = {Levy, EJ and Zipple, MN and McLean, E and Campos, FA and Dasari, M and Fogel, AS and Franz, M and Gesquiere, LR and Gordon, JB and Grieneisen, L and Habig, B and Jansen, DJ and Learn, NH and Weibel, CJ and Altmann, J and Alberts, SC and Archie, EA}, Title = {A comparison of dominance rank metrics reveals multiple competitive landscapes in an animal society.}, Journal = {Proceedings. Biological sciences}, Volume = {287}, Number = {1934}, Pages = {20201013}, Year = {2020}, Month = {September}, url = {http://dx.doi.org/10.1098/rspb.2020.1013}, Abstract = {Across group-living animals, linear dominance hierarchies lead to disparities in access to resources, health outcomes and reproductive performance. Studies of how dominance rank predicts these traits typically employ one of several dominance rank metrics without examining the assumptions each metric makes about its underlying competitive processes. Here, we compare the ability of two dominance rank metrics-simple ordinal rank and proportional or 'standardized' rank-to predict 20 traits in a wild baboon population in Amboseli, Kenya. We propose that simple ordinal rank best predicts traits when competition is density-dependent, whereas proportional rank best predicts traits when competition is density-independent. We found that for 75% of traits (15/20), one rank metric performed better than the other. Strikingly, all male traits were best predicted by simple ordinal rank, whereas female traits were evenly split between proportional and simple ordinal rank. Hence, male and female traits are shaped by different competitive processes: males are largely driven by density-dependent resource access (e.g. access to oestrous females), whereas females are shaped by both density-independent (e.g. distributed food resources) and density-dependent resource access. This method of comparing how different rank metrics predict traits can be used to distinguish between different competitive processes operating in animal societies.}, Doi = {10.1098/rspb.2020.1013}, Key = {fds352212} } @article{fds351177, Author = {Rosenbaum, S and Zeng, S and Campos, FA and Gesquiere, LR and Altmann, J and Alberts, SC and Li, F and Archie, EA}, Title = {Social bonds do not mediate the relationship between early adversity and adult glucocorticoids in wild baboons.}, Journal = {Proceedings of the National Academy of Sciences of the United States of America}, Volume = {117}, Number = {33}, Pages = {20052-20062}, Year = {2020}, Month = {August}, url = {http://dx.doi.org/10.1073/pnas.2004524117}, Abstract = {In humans and other animals, harsh conditions in early life can have profound effects on adult physiology, including the stress response. This relationship may be mediated by a lack of supportive relationships in adulthood. That is, early life adversity may inhibit the formation of supportive social ties, and weak social support is itself often linked to dysregulated stress responses. Here, we use prospective, longitudinal data from wild baboons in Kenya to test the links between early adversity, adult social bonds, and adult fecal glucocorticoid hormone concentrations (a measure of hypothalamic-pituitary-adrenal [HPA] axis activation and the stress response). Using a causal inference framework, we found that experiencing one or more sources of early adversity led to a 9 to 14% increase in females' glucocorticoid concentrations across adulthood. However, these effects were not mediated by weak social bonds: The direct effects of early adversity on adult glucocorticoid concentrations were 11 times stronger than the effects mediated by social bonds. This pattern occurred, in part, because the effect of social bonds on glucocorticoids was weak compared to the powerful effects of early adversity on glucocorticoid levels in adulthood. Hence, in female baboons, weak social bonds in adulthood are not enough to explain the effects of early adversity on glucocorticoid concentrations. Together, our results support the well-established notions that early adversity and weak social bonds both predict poor adult health. However, the magnitudes of these two effects differ considerably, and they may act independently of one another.}, Doi = {10.1073/pnas.2004524117}, Key = {fds351177} } @article{fds352728, Author = {Noonan, MJ and Fleming, CH and Tucker, MA and Kays, R and Harrison, A-L and Crofoot, MC and Abrahms, B and Alberts, SC and Ali, AH and Altmann, J and Antunes, PC and Attias, N and Belant, JL and Beyer, DE and Bidner, LR and Blaum, N and Boone, RB and Caillaud, D and de Paula, RC and de la Torre, JA and Dekker, J and DePerno, CS and Farhadinia, M and Fennessy, J and Fichtel, C and Fischer, C and Ford, A and Goheen, JR and Havmøller, RW and Hirsch, BT and Hurtado, C and Isbell, LA and Janssen, R and Jeltsch, F and Kaczensky, P and Kaneko, Y and Kappeler, P and Katna, A and Kauffman, M and Koch, F and Kulkarni, A and LaPoint, S and Leimgruber, P and Macdonald, DW and Markham, AC and McMahon, L and Mertes, K and Moorman, CE and Morato, RG and Moßbrucker, AM and Mourão, G and O'Connor, D and Oliveira-Santos, LGR and Pastorini, J and Patterson, BD and Rachlow, J and Ranglack, DH and Reid, N and Scantlebury, DM and Scott, DM and Selva, N and Sergiel, A and Songer, M and Songsasen, N and Stabach, JA and Stacy-Dawes, J and Swingen, MB and Thompson, JJ and Ullmann, W and Vanak, AT and Thaker, M and Wilson, JW and Yamazaki, K and Yarnell, RW and Zieba, F and Zwijacz-Kozica, T and Fagan, WF and Mueller, T and Calabrese, JM}, Title = {Effects of body size on estimation of mammalian area requirements.}, Journal = {Conservation biology : the journal of the Society for Conservation Biology}, Volume = {34}, Number = {4}, Pages = {1017-1028}, Year = {2020}, Month = {August}, url = {http://dx.doi.org/10.1111/cobi.13495}, Abstract = {Accurately quantifying species' area requirements is a prerequisite for effective area-based conservation. This typically involves collecting tracking data on species of interest and then conducting home-range analyses. Problematically, autocorrelation in tracking data can result in space needs being severely underestimated. Based on the previous work, we hypothesized the magnitude of underestimation varies with body mass, a relationship that could have serious conservation implications. To evaluate this hypothesis for terrestrial mammals, we estimated home-range areas with global positioning system (GPS) locations from 757 individuals across 61 globally distributed mammalian species with body masses ranging from 0.4 to 4000 kg. We then applied block cross-validation to quantify bias in empirical home-range estimates. Area requirements of mammals <10 kg were underestimated by a mean approximately15%, and species weighing approximately100 kg were underestimated by approximately50% on average. Thus, we found area estimation was subject to autocorrelation-induced bias that was worse for large species. Combined with the fact that extinction risk increases as body mass increases, the allometric scaling of bias we observed suggests the most threatened species are also likely to be those with the least accurate home-range estimates. As a correction, we tested whether data thinning or autocorrelation-informed home-range estimation minimized the scaling effect of autocorrelation on area estimates. Data thinning required an approximately93% data loss to achieve statistical independence with 95% confidence and was, therefore, not a viable solution. In contrast, autocorrelation-informed home-range estimation resulted in consistently accurate estimates irrespective of mass. When relating body mass to home range size, we detected that correcting for autocorrelation resulted in a scaling exponent significantly >1, meaning the scaling of the relationship changed substantially at the upper end of the mass spectrum.}, Doi = {10.1111/cobi.13495}, Key = {fds352728} } @article{fds349640, Author = {Snyder-Mackler, N and Burger, JR and Gaydosh, L and Belsky, DW and Noppert, GA and Campos, FA and Bartolomucci, A and Yang, YC and Aiello, AE and O'Rand, A and Harris, KM and Shively, CA and Alberts, SC and Tung, J}, Title = {Social determinants of health and survival in humans and other animals.}, Journal = {Science (New York, N.Y.)}, Volume = {368}, Number = {6493}, Pages = {eaax9553}, Year = {2020}, Month = {May}, url = {http://dx.doi.org/10.1126/science.aax9553}, Abstract = {The social environment, both in early life and adulthood, is one of the strongest predictors of morbidity and mortality risk in humans. Evidence from long-term studies of other social mammals indicates that this relationship is similar across many species. In addition, experimental studies show that social interactions can causally alter animal physiology, disease risk, and life span itself. These findings highlight the importance of the social environment to health and mortality as well as Darwinian fitness-outcomes of interest to social scientists and biologists alike. They thus emphasize the utility of cross-species analysis for understanding the predictors of, and mechanisms underlying, social gradients in health.}, Doi = {10.1126/science.aax9553}, Key = {fds349640} } @article{fds349049, Author = {Gesquiere, LR and Habig, B and Hansen, C and Li, A and Freid, K and Learn, NH and Alberts, SC and Graham, AL and Archie, EA}, Title = {Noninvasive measurement of mucosal immunity in a free-ranging baboon population.}, Journal = {American journal of primatology}, Volume = {82}, Number = {2}, Pages = {e23093}, Year = {2020}, Month = {February}, url = {http://dx.doi.org/10.1002/ajp.23093}, Abstract = {Ecoimmunological patterns and processes remain understudied in wild primates, in part because of the lack of noninvasive methods to measure immunity. Secretory immunoglobulin A (sIgA) is the most abundant antibody present at mammalian mucosal surfaces and provides an important first line of defense against pathogens. Recent studies show that sIgA can be measured noninvasively in feces and is a good marker of mucosal immunity. Here we validated a commercial ELISA kit to measure fecal IgA in baboons, tested the robustness of its results to variation in collection and storage conditions, and developed a cost-effective in-house ELISA for baboon fecal IgA. Using data from the custom ELISA, we assessed the relationship between fecal IgA concentrations and gastrointestinal parasite burden, and tested how sex, age, and reproductive effort predict fecal IgA in wild baboons. We find that IgA concentrations can be measured in baboon feces using an in-house ELISA and are highly correlated to the values obtained with a commercial kit. Fecal IgA concentrations are stable when extracts are stored for up to 22 months at -20°C. Fecal IgA concentrations were negatively correlated with parasite egg counts (Trichuris trichiura), but not parasite richness. Fecal IgA did not vary between the sexes, but for males, concentrations were higher in adults versus adolescents. Lactating females had significantly lower fecal IgA than pregnant females, but neither pregnant nor lactating female concentrations differed significantly from cycling females. Males who engaged in more mate-guarding exhibited similar IgA concentrations to those who engaged in little mate-guarding. These patterns may reflect the low energetic costs of mucosal immunity, or the complex dependence of IgA excretion on individual condition. Adding a noninvasive measure of mucosal immunity will promote a better understanding of how ecology modulates possible tradeoffs between the immune system and other energetically costly processes in the wild.}, Doi = {10.1002/ajp.23093}, Key = {fds349049} } @article{fds363029, Author = {Fogel, A and McLean, E and Gordon, J and Archie, E and Tung, J and Alberts, S}, Title = {Genetic ancestry predicts male-female affiliation in a natural baboon hybrid zone}, Year = {2020}, url = {http://dx.doi.org/10.1101/2020.10.28.358002}, Abstract = {<h4>ABSTRACT</h4> Opposite-sex social relationships are important predictors of fitness in many animals, including several group-living mammals. Consequently, understanding sources of variance in the tendency to form opposite-sex relationships is important for understanding social evolution. Genetic contributions are of particular interest due to their importance in long-term evolutionary change, but little is known about genetic effects on male-female relationships in social mammals, especially outside of the mating context. Here, we investigate the effects of genetic ancestry on male-female affiliative behavior in a hybrid zone between the yellow baboon ( Papio cynocephalus ) and the anubis baboon ( P. anubis ), in a population in which male-female social bonds are known predictors of lifespan. We place our analysis within the context of other social and demographic predictors of affiliative behavior in baboons. Genetic ancestry was the most consistent predictor of opposite-sex affiliative behavior we observed, with the exception of strong effects of dominance rank. Our results show that increased anubis genetic ancestry is associated with subtly, but significantly higher rates of opposite-sex affiliative behavior, in both males and females. Additionally, pairs of anubis-like males and anubis-like females were the most likely to socially affiliate, resulting in moderate assortativity in grooming and proximity behavior as a function of genetic ancestry. Our findings indicate that opposite-sex affiliative behavior partially diverged during baboon evolution to differentiate yellow and anubis baboons, despite overall similarities in their social structures and mating systems. Further, they suggest that affiliative behavior may simultaneously promote and constrain baboon admixture, through additive and assortative effects of ancestry, respectively. <h4>HIGHLIGHTS</h4> Opposite-sex social relationships can have important fitness consequences. In hybrid baboons, genetic ancestry predicted male-female affiliative behavior. Both an individual’s genetic ancestry and that of its social partner mattered. Male-female affiliation was assortative with respect to genetic ancestry. Dominance rank and group demography also influenced male-female social affiliation.}, Doi = {10.1101/2020.10.28.358002}, Key = {fds363029} } @article{fds363829, Author = {Anderson, J and Johnston, R and Lea, A and Campos, F and Voyles, T and Akinyi, M and Alberts, S and Archie, E and Tung, J}, Title = {The costs of competition: high social status males experience accelerated epigenetic aging in wild baboons}, Year = {2020}, url = {http://dx.doi.org/10.1101/2020.02.22.961052}, Abstract = {Aging, for virtually all life, is inescapable. However, within populations, biological aging rates vary. Understanding sources of variation in this process is central to understanding the biodemography of natural populations. We constructed a DNA methylation-based age predictor for an intensively studied wild baboon population in Kenya. Consistent with findings in humans, the resulting “epigenetic clock” closely tracks chronological age, but individuals are predicted to be somewhat older or younger than their known ages. Surprisingly, these deviations are not explained by the strongest predictors of lifespan in this population, early adversity and social integration. Instead, they are best predicted by male dominance rank: high-ranking males are predicted to be older than their true ages, and epigenetic age tracks changes in rank over time. Our results argue that achieving high rank for male baboons—the best predictor of reproductive success—imposes costs consistent with a “live fast, die young” life history strategy.}, Doi = {10.1101/2020.02.22.961052}, Key = {fds363829} } @article{fds349050, Author = {McLean, EM and Archie, EA and Alberts, SC}, Title = {Lifetime Fitness in Wild Female Baboons: Trade-Offs and Individual Heterogeneity in Quality.}, Journal = {The American naturalist}, Volume = {194}, Number = {6}, Pages = {745-759}, Year = {2019}, Month = {December}, url = {http://dx.doi.org/10.1086/705810}, Abstract = {Understanding the evolution of life histories requires information on how life histories vary among individuals and how such variation predicts individual fitness. Using complete life histories for females in a well-studied population of wild baboons, we tested two nonexclusive hypotheses about the relationships among survival, reproduction, and fitness: the quality hypothesis, which predicts positive correlations between life-history traits, mediated by variation in resource acquisition, and the trade-off hypothesis, which predicts negative correlations between life-history traits, mediated by trade-offs in resource allocation. In support of the quality hypothesis, we found that females with higher rates of offspring survival were themselves better at surviving. Further, after statistically controlling for variation in female quality, we found evidence for two types of trade-offs: females who produced surviving offspring at a slower rate had longer life spans than those who produced surviving offspring at a faster rate, and females who produced surviving offspring at a slower rate had a higher overall proportion of offspring survive infancy than females who produced surviving offspring at a faster rate. Importantly, these trade-offs were evident even when accounting for (i) the influence of offspring survival on maternal birth rate, (ii) the dependence of offspring survival on maternal survival, and (iii) potential age-related changes in birth rate and/or offspring survival. Our results shed light on why trade-offs are evident in some populations while variation in individual quality masks trade-offs in others.}, Doi = {10.1086/705810}, Key = {fds349050} } @article{fds347006, Author = {Fischer, J and Higham, JP and Alberts, SC and Barrett, L and Beehner, JC and Bergman, TJ and Carter, AJ and Collins, A and Elton, S and Fagot, J and Ferreira da Silva and MJ and Hammerschmidt, K and Henzi, P and Jolly, CJ and Knauf, S and Kopp, GH and Rogers, J and Roos, C and Ross, C and Seyfarth, RM and Silk, J and Snyder-Mackler, N and Staedele, V and Swedell, L and Wilson, ML and Zinner, D}, Title = {Insights into the evolution of social systems and species from baboon studies.}, Journal = {eLife}, Volume = {8}, Pages = {e50989}, Year = {2019}, Month = {November}, url = {http://dx.doi.org/10.7554/elife.50989}, Abstract = {Baboons, members of the genus <i>Papio,</i> comprise six closely related species distributed throughout sub-Saharan Africa and southwest Arabia. The species exhibit more ecological flexibility and a wider range of social systems than many other primates. This article summarizes our current knowledge of the natural history of baboons and highlights directions for future research. We suggest that baboons can serve as a valuable model for complex evolutionary processes, such as speciation and hybridization. The evolution of baboons has been heavily shaped by climatic changes and population expansion and fragmentation in the African savanna environment, similar to the processes that acted during human evolution. With accumulating long-term data, and new data from previously understudied species, baboons are ideally suited for investigating the links between sociality, health, longevity and reproductive success. To achieve these aims, we propose a closer integration of studies at the proximate level, including functional genomics, with behavioral and ecological studies.}, Doi = {10.7554/elife.50989}, Key = {fds347006} } @article{fds349051, Author = {Habig, B and Jansen, DAWAM and Akinyi, MY and Gesquiere, LR and Alberts, SC and Archie, EA}, Title = {Multi-scale predictors of parasite risk in wild male savanna baboons (Papio cynocephalus)}, Journal = {Behavioral Ecology and Sociobiology}, Volume = {73}, Number = {10}, Publisher = {Springer Science and Business Media LLC}, Year = {2019}, Month = {October}, url = {http://dx.doi.org/10.1007/s00265-019-2748-y}, Abstract = {Abstract: Several factors are thought to shape male parasite risk in polygynous and polygynandrous mammals, including male-male competition, investment in potentially immunosuppressive hormones, and dispersal. Parasitism is also driven by processes occurring at larger scales, including host social groups and populations. To date, studies that test parasite-related costs of male behavior at all three scales—individual hosts, social groups, and the host population—remain rare. To fill this gap, we investigated multi-scale predictors of helminth parasitism in 97 male savanna baboons (Papio cynocephalus) living in the Amboseli ecosystem in Kenya over a 5-year span. Controlling for multi-scale processes, we found that many of the classic indicators of male mating effort—high dominance rank, testosterone, and glucocorticoids—did not predict helminth infection risk. However, we identified two parasite-related costs associated with male behavior: (i) socially connected males exhibited higher Trichuris trichiura egg counts and greater parasite species richness than socially isolated males and (ii) males with stable group residency exhibited higher parasite species richness than males who frequently dispersed to new social groups. At the population level, males harbored more parasites following periods of drought than rainfall. Lastly, parasites exhibited positive covariance suggesting that infection risk increases if a host already harbors one or more parasite taxa. These results indicate that multi-scale processes are important in driving male parasite risk and that some aspects of male behavior are costly. Together, our results provide an unusually holistic perspective on the drivers of parasite risk in the context of male behaviors and life histories. Significance statement: Infection by gastrointestinal helminths can have major consequences for host fitness, especially in the context of male mating effort. Multi-scale processes—from the host to its social group and population—are important for understanding key drivers of parasitism. We leveraged long-term data from one of the longest running behavioral ecology studies of a wild primate population in the world, the well-studied Amboseli baboon population in Kenya. We found that traditional indicators of male mating effort (attaining high dominance rank, high testosterone and glucocorticoids) did not predict parasitism. However, male social connectedness to females, competitive group demography, and harsh weather were all associated with higher parasitism. Because socially connected males faced the highest parasite risk, males may face a tradeoff between male-female relationships and parasitism. Our results show how processes at multiple scales contribute to variation in male parasite risk.}, Doi = {10.1007/s00265-019-2748-y}, Key = {fds349051} } @article{fds346370, Author = {Zipple, MN and Archie, EA and Tung, J and Altmann, J and Alberts, SC}, Title = {Intergenerational effects of early adversity on survival in wild baboons.}, Journal = {eLife}, Volume = {8}, Pages = {e47433}, Year = {2019}, Month = {September}, url = {http://dx.doi.org/10.7554/elife.47433}, Abstract = {Early life adversity can affect an individual's health, survival, and fertility for many years after the adverse experience. Whether early life adversity also imposes intergenerational effects on the exposed individual's offspring is not well understood. We fill this gap by leveraging prospective, longitudinal data on a wild, long-lived primate. We find that juveniles whose mothers experienced early life adversity exhibit high mortality before age 4, independent of the juvenile's own experience of early adversity. These juveniles often preceded their mothers in death by 1 to 2 years, indicating that high adversity females decline in their ability to raise offspring near the end of life. While we cannot exclude direct effects of a parent's environment on offspring quality (e.g., inherited epigenetic changes), our results are completely consistent with a classic parental effect, in which the environment experienced by a parent affects its future phenotype and therefore its offspring's phenotype.}, Doi = {10.7554/elife.47433}, Key = {fds346370} } @article{fds343201, Author = {Akinyi, MY and Jansen, D and Habig, B and Gesquiere, LR and Alberts, SC and Archie, EA}, Title = {Costs and drivers of helminth parasite infection in wild female baboons.}, Journal = {The Journal of animal ecology}, Volume = {88}, Number = {7}, Pages = {1029-1043}, Year = {2019}, Month = {July}, url = {http://dx.doi.org/10.1111/1365-2656.12994}, Abstract = {Helminth parasites can have wide-ranging, detrimental effects on host reproduction and survival. These effects are best documented in humans and domestic animals, while only a few studies in wild mammals have identified both the forces that drive helminth infection risk and their costs to individual fitness. Working in a well-studied population of wild baboons (Papio cynocephalus) in the Amboseli ecosystem in Kenya, we pursued two goals, to (a) examine the costs of helminth infections in terms of female fertility and glucocorticoid hormone levels and (b) test how processes operating at multiple scales-from individual hosts to social groups and the population at large-work together to predict variation in female infection risk. To accomplish these goals, we measured helminth parasite burdens in 745 faecal samples collected over 5 years from 122 female baboons. We combine these data with detailed observations of host environments, social behaviours, hormone levels and interbirth intervals (IBIs). We found that helminths are costly to female fertility: females infected with more diverse parasite communities (i.e., higher parasite richness) exhibited longer IBIs than females infected by fewer parasite taxa. We also found that females exhibiting high Trichuris trichiura egg counts also had high glucocorticoid levels. Female infection risk was best predicted by factors at the host, social group and population level: females facing the highest risk were old, socially isolated, living in dry conditions and infected with other helminths. Our results provide an unusually holistic understanding of the factors that contribute to inter-individual differences in parasite infection, and they contribute to just a handful of studies linking helminths to host fitness in wild mammals.}, Doi = {10.1111/1365-2656.12994}, Key = {fds343201} } @article{fds341322, Author = {Noonan, MJ and Tucker, MA and Fleming, CH and Akre, TS and Alberts, SC and Ali, AH and Altmann, J and Antunes, PC and Belant, JL and Beyer, D and Blaum, N and Böhning-Gaese, K and Cullen, L and de Paula, RC and Dekker, J and Drescher-Lehman, J and Farwig, N and Fichtel, C and Fischer, C and Ford, AT and Goheen, JR and Janssen, R and Jeltsch, F and Kauffman, M and Kappeler, PM and Koch, F and LaPoint, S and Markham, AC and Medici, EP and Morato, RG and Nathan, R and Oliveira-Santos, LGR and Olson, KA and Patterson, BD and Paviolo, A and Ramalho, EE and Rösner, S and Schabo, DG and Selva, N and Sergiel, A and Xavier da Silva and M and Spiegel, O and Thompson, P and Ullmann, W and Zięba, F and Zwijacz-Kozica, T and Fagan, WF and Mueller, T and Calabrese, JM}, Title = {A comprehensive analysis of autocorrelation and bias in home range estimation}, Journal = {Ecological Monographs}, Volume = {89}, Number = {2}, Year = {2019}, Month = {May}, url = {http://dx.doi.org/10.1002/ecm.1344}, Abstract = {Home range estimation is routine practice in ecological research. While advances in animal tracking technology have increased our capacity to collect data to support home range analysis, these same advances have also resulted in increasingly autocorrelated data. Consequently, the question of which home range estimator to use on modern, highly autocorrelated tracking data remains open. This question is particularly relevant given that most estimators assume independently sampled data. Here, we provide a comprehensive evaluation of the effects of autocorrelation on home range estimation. We base our study on an extensive data set of GPS locations from 369 individuals representing 27 species distributed across five continents. We first assemble a broad array of home range estimators, including Kernel Density Estimation (KDE) with four bandwidth optimizers (Gaussian reference function, autocorrelated-Gaussian reference function [AKDE], Silverman's rule of thumb, and least squares cross-validation), Minimum Convex Polygon, and Local Convex Hull methods. Notably, all of these estimators except AKDE assume independent and identically distributed (IID) data. We then employ half-sample cross-validation to objectively quantify estimator performance, and the recently introduced effective sample size for home range area estimation ((Formula presented.)) to quantify the information content of each data set. We found that AKDE 95% area estimates were larger than conventional IID-based estimates by a mean factor of 2. The median number of cross-validated locations included in the hold-out sets by AKDE 95% (or 50%) estimates was 95.3% (or 50.1%), confirming the larger AKDE ranges were appropriately selective at the specified quantile. Conversely, conventional estimates exhibited negative bias that increased with decreasing (Formula presented.). To contextualize our empirical results, we performed a detailed simulation study to tease apart how sampling frequency, sampling duration, and the focal animal's movement conspire to affect range estimates. Paralleling our empirical results, the simulation study demonstrated that AKDE was generally more accurate than conventional methods, particularly for small (Formula presented.). While 72% of the 369 empirical data sets had >1,000 total observations, only 4% had an (Formula presented.) >1,000, where 30% had an (Formula presented.) <30. In this frequently encountered scenario of small (Formula presented.), AKDE was the only estimator capable of producing an accurate home range estimate on autocorrelated data.}, Doi = {10.1002/ecm.1344}, Key = {fds341322} } @article{fds342537, Author = {Zipple, MN and Roberts, EK and Alberts, SC and Beehner, JC}, Title = {Male-mediated prenatal loss: Functions and mechanisms.}, Journal = {Evolutionary anthropology}, Volume = {28}, Number = {3}, Pages = {114-125}, Year = {2019}, Month = {May}, url = {http://dx.doi.org/10.1002/evan.21776}, Abstract = {Sexually selected infanticide has been the subject of intense empirical and theoretical study for decades; a related phenomenon, male-mediated prenatal loss, has received much less attention in evolutionary studies. Male-mediated prenatal loss occurs when inseminated or pregnant females terminate reproductive effort following exposure to a nonsire male, either through implantation failure or pregnancy termination. Male-mediated prenatal loss encompasses two sub-phenomena: sexually selected feticide and the Bruce effect. In this review, we provide a framework that explains the relationship between feticide and the Bruce effect and describes what is known about the proximate and ultimate mechanisms involved in each. Using a simple model, we demonstrate that male-mediated prenatal loss can provide greater reproductive benefits to males than infanticide. We therefore suggest that, compared to infanticide, male-mediated prenatal loss may be more prevalent in mammalian species and may have played a greater role in their social evolution than has previously been documented.}, Doi = {10.1002/evan.21776}, Key = {fds342537} } @article{fds342749, Author = {Grieneisen, LE and Charpentier, MJE and Alberts, SC and Blekhman, R and Bradburd, G and Tung, J and Archie, EA}, Title = {Genes, geology and germs: gut microbiota across a primate hybrid zone are explained by site soil properties, not host species.}, Journal = {Proceedings. Biological sciences}, Volume = {286}, Number = {1901}, Pages = {20190431}, Year = {2019}, Month = {April}, url = {http://dx.doi.org/10.1098/rspb.2019.0431}, Abstract = {Gut microbiota in geographically isolated host populations are often distinct. These differences have been attributed to between-population differences in host behaviours, environments, genetics and geographical distance. However, which factors are most important remains unknown. Here, we fill this gap for baboons by leveraging information on 13 environmental variables from 14 baboon populations spanning a natural hybrid zone. Sampling across a hybrid zone allowed us to additionally test whether phylosymbiosis (codiversification between hosts and their microbiota) is detectable in admixed, closely related primates. We found little evidence of genetic effects: none of host genetic ancestry, host genetic relatedness nor genetic distance between host populations were strong predictors of baboon gut microbiota. Instead, gut microbiota were best explained by the baboons' environments, especially the soil's geologic history and exchangeable sodium. Indeed, soil effects were 15 times stronger than those of host-population F<sub>ST,</sub> perhaps because soil predicts which foods are present, or because baboons are terrestrial and consume soil microbes incidentally with their food. Our results support an emerging picture in which environmental variation is the dominant predictor of host-associated microbiomes. We are the first to show that such effects overshadow host species identity among members of the same primate genus.}, Doi = {10.1098/rspb.2019.0431}, Key = {fds342749} } @article{fds340889, Author = {Wango, TL and Musiega, D and Mundia, CN and Altmann, J and Alberts, SC and Tung, J}, Title = {Climate and Land Cover Analysis Suggest No Strong Ecological Barriers to Gene Flow in a Natural Baboon Hybrid Zone}, Journal = {International Journal of Primatology}, Volume = {40}, Number = {1}, Pages = {53-70}, Year = {2019}, Month = {February}, url = {http://dx.doi.org/10.1007/s10764-017-9989-2}, Abstract = {Admixture between diverging taxa has made, and continues to make, an important contribution to primate diversity and evolution. However, although naturally occurring hybrids have now been documented in all major primate lineages, we still know relatively little about the factors that shape when and where admixture occurs. Baboons (genus Papio), in which multiple natural hybrid zones are well described, provide a valuable system to investigate these factors. Here, we combined Geographic Information Systems and weather station data with information on genetically characterized populations in southern Kenya to investigate if ecological variables present a potential barrier to gene flow between anubis baboons and yellow baboons in the region. Specifically, we asked if altitude, seasonal temperature, or seasonal precipitation differ for weather stations in anubis, yellow, or hybrid ranges in southern Kenya, and if land cover or altitude covary with population ancestry near the hybrid zone. Our analyses suggest that the range of yellow baboons in Kenya is climatically distinct from the range of anubis baboons, with hybrids in intermediate regions. However, we identified no clear pattern of climate or land cover differentiation near the hybrid zone itself. Thus, when yellow baboons and anubis baboons come into contact, our data suggest that the resulting population composition is not consistently predicted by the ecological variables we considered. Our results support the designation of baboons as highly flexible “generalists,” and suggest that more fine-grained analyses (e.g., relative success in ecologically stressful years) may be necessary to detect clear signals of ecological barriers to gene flow.}, Doi = {10.1007/s10764-017-9989-2}, Key = {fds340889} } @article{fds340427, Author = {Colchero, F and Jones, OR and Conde, DA and Hodgson, D and Zajitschek, F and Schmidt, BR and Malo, AF and Alberts, SC and Becker, PH and Bouwhuis, S and Bronikowski, AM and De Vleeschouwer and KM and Delahay, RJ and Dummermuth, S and Fernández-Duque, E and Frisenvaenge, J and Hesselsøe, M and Larson, S and Lemaître, J-F and McDonald, J and Miller, DAW and O'Donnell, C and Packer, C and Raboy, BE and Reading, CJ and Wapstra, E and Weimerskirch, H and While, GM and Baudisch, A and Flatt, T and Coulson, T and Gaillard, J-M}, Title = {The diversity of population responses to environmental change.}, Journal = {Ecology letters}, Volume = {22}, Number = {2}, Pages = {342-353}, Year = {2019}, Month = {February}, url = {http://dx.doi.org/10.1111/ele.13195}, Abstract = {The current extinction and climate change crises pressure us to predict population dynamics with ever-greater accuracy. Although predictions rest on the well-advanced theory of age-structured populations, two key issues remain poorly explored. Specifically, how the age-dependency in demographic rates and the year-to-year interactions between survival and fecundity affect stochastic population growth rates. We use inference, simulations and mathematical derivations to explore how environmental perturbations determine population growth rates for populations with different age-specific demographic rates and when ages are reduced to stages. We find that stage- vs. age-based models can produce markedly divergent stochastic population growth rates. The differences are most pronounced when there are survival-fecundity-trade-offs, which reduce the variance in the population growth rate. Finally, the expected value and variance of the stochastic growth rates of populations with different age-specific demographic rates can diverge to the extent that, while some populations may thrive, others will inevitably go extinct.}, Doi = {10.1111/ele.13195}, Key = {fds340427} } @article{fds335219, Author = {Alberts, SC}, Title = {Social influences on survival and reproduction: Insights from a long-term study of wild baboons.}, Journal = {The Journal of animal ecology}, Volume = {88}, Number = {1}, Pages = {47-66}, Year = {2019}, Month = {January}, url = {http://dx.doi.org/10.1111/1365-2656.12887}, Abstract = {For social species, the environment has two components: physical and social. The social environment modifies the individual's interaction with the physical environment, and the physical environment may in turn impact individuals' social relationships. This interplay can generate considerable variation among individuals in survival and reproduction. Here, I synthesize more than four decades of research on the baboons of the Amboseli basin in southern Kenya to illustrate how social and physical environments interact to affect reproduction and survival. For immature baboons, social behaviour can both mitigate and exacerbate the challenge of survival. Only c. 50% of live-born females and c. 44% of live-born males reach the median age of first reproduction. Variation in pre-adult survival, growth and development is associated with multiple aspects of the social environment. For instance, conspecifics provide direct care and are a major source of social knowledge about food and the environment, but conspecifics can also represent a direct threat to survival through infanticide. In adulthood, both competition (within and between social groups) and cooperative affiliation (i.e. collective action and/or the exchange of social resources such as grooming) are prominent features of baboon social life and have important consequences for reproduction and survival. For instance, adult females with higher social dominance ranks have accelerated reproduction, and adult females that engage in more frequent affiliative social interactions have higher survival throughout adulthood. The early life environment also has important consequences for adult reproduction and survival, as in a number of other bird and mammal species. In seasonal breeders, early life effects often apply to entire cohorts; in contrast, in nonseasonal and highly social species such as baboons, early life effects are more individual-specific, stemming from considerable variation not only in the early physical environment (even if they are born in the same year) but also in the particulars of their social environment.}, Doi = {10.1111/1365-2656.12887}, Key = {fds335219} } @article{fds339382, Author = {Reese, AT and Pereira, FC and Schintlmeister, A and Berry, D and Wagner, M and Hale, LP and Wu, A and Jiang, S and Durand, HK and Zhou, X and Premont, RT and Diehl, AM and O'Connell, TM and Alberts, SC and Kartzinel, TR and Pringle, RM and Dunn, RR and Wright, JP and David, LA}, Title = {Microbial nitrogen limitation in the mammalian large intestine.}, Journal = {Nat Microbiol}, Volume = {3}, Number = {12}, Pages = {1441-1450}, Year = {2018}, Month = {December}, url = {http://dx.doi.org/10.1038/s41564-018-0267-7}, Abstract = {Resource limitation is a fundamental factor governing the composition and function of ecological communities. However, the role of resource supply in structuring the intestinal microbiome has not been established and represents a challenge for mammals that rely on microbial symbionts for digestion: too little supply might starve the microbiome while too much might starve the host. We present evidence that microbiota occupy a habitat that is limited in total nitrogen supply within the large intestines of 30 mammal species. Lowering dietary protein levels in mice reduced their faecal concentrations of bacteria. A gradient of stoichiometry along the length of the gut was consistent with the hypothesis that intestinal nitrogen limitation results from host absorption of dietary nutrients. Nitrogen availability is also likely to be shaped by host-microbe interactions: levels of host-secreted nitrogen were altered in germ-free mice and when bacterial loads were reduced via experimental antibiotic treatment. Single-cell spectrometry revealed that members of the phylum Bacteroidetes consumed nitrogen in the large intestine more readily than other commensal taxa did. Our findings support a model where nitrogen limitation arises from preferential host use of dietary nutrients. We speculate that this resource limitation could enable hosts to regulate microbial communities in the large intestine. Commensal microbiota may have adapted to nitrogen-limited settings, suggesting one reason why excess dietary protein has been associated with degraded gut-microbial ecosystems.}, Doi = {10.1038/s41564-018-0267-7}, Key = {fds339382} } @article{fds340052, Author = {Lea, AJ and Akinyi, MY and Nyakundi, R and Mareri, P and Nyundo, F and Kariuki, T and Alberts, SC and Archie, EA and Tung, J}, Title = {Dominance rank-associated gene expression is widespread, sex-specific, and a precursor to high social status in wild male baboons.}, Journal = {Proceedings of the National Academy of Sciences of the United States of America}, Volume = {115}, Number = {52}, Pages = {E12163-E12171}, Year = {2018}, Month = {December}, url = {http://dx.doi.org/10.1073/pnas.1811967115}, Abstract = {In humans and other hierarchical species, social status is tightly linked to variation in health and fitness-related traits. Experimental manipulations of social status in female rhesus macaques suggest that this relationship is partially explained by status effects on immune gene regulation. However, social hierarchies are established and maintained in different ways across species: While some are based on kin-directed nepotism, others emerge from direct physical competition. We investigated how this variation influences the relationship between social status and immune gene regulation in wild baboons, where hierarchies in males are based on fighting ability but female hierarchies are nepotistic. We measured rank-related variation in gene expression levels in adult baboons of both sexes at baseline and in response to ex vivo stimulation with the bacterial endotoxin lipopolysaccharide (LPS). We identified >2,000 rank-associated genes in males, an order of magnitude more than in females. In males, high status predicted increased expression of genes involved in innate immunity and preferential activation of the NF-κB-mediated proinflammatory pathway, a pattern previously associated with low status in female rhesus macaques. Using Mendelian randomization, we reconcile these observations by demonstrating that high status-associated gene expression patterns are precursors, not consequences, of high social status in males, in support of the idea that physiological condition determines who attains high rank. Together, our work provides a test of the relationship between social status and immune gene regulation in wild primates. It also emphasizes the importance of social context in shaping the relationship between social status and immune function.}, Doi = {10.1073/pnas.1811967115}, Key = {fds340052} } @article{fds332674, Author = {Gesquiere, LR and Altmann, J and Archie, EA and Alberts, SC}, Title = {Interbirth intervals in wild baboons: Environmental predictors and hormonal correlates.}, Journal = {American journal of physical anthropology}, Volume = {166}, Number = {1}, Pages = {107-126}, Year = {2018}, Month = {May}, url = {http://dx.doi.org/10.1002/ajpa.23407}, Abstract = {<h4>Objectives</h4>Interbirth intervals (IBIs) are a key metric of female reproductive success; understanding how they are regulated by environmental, social, and demographic factors can provide insight into sources of variance in female fitness.<h4>Materials and methods</h4>Using 36 years of reproductive data on 490 IBIs for 160 wild female baboons, we identified sources of variance in the duration of IBIs and of their component phases: postpartum amenorrhea (PPA), sexual cycling, and pregnancy. We also examined how body fat and fecal hormone concentrations varied during female IBIs.<h4>Results</h4>We found that IBIs tended to be shorter (reproduction was accelerated) when female traits and environmental variables promoted energy acquisition, but with different specific effects for different component phases of the IBI. We also found that females lost a substantial amount of body fat during PPA, indicating that PPA imposes accumulating energetic costs as it progresses. Prior to cycle resumption females began to regain body fat; body fat was stable across the cycling phase and increased throughout most of pregnancy. However, body fat scores per se were not associated with the duration of any of the component phases. Finally, we found that fecal glucocorticoid concentrations decreased as PPA progressed, suggesting a decline in energetic stress over this phase. Fecal progestogen and estrogen concentrations changed over time during sexual cycling; the direction of these changes depended on the phase of the sexual cycle (luteal versus early or late follicular phases).<h4>Discussion</h4>Our study lends insight into the energetic constraints on female primate reproduction, revealing how female environments, changes in body fat, and steroid hormone concentrations relate to IBI duration and to reproductive readiness.}, Doi = {10.1002/ajpa.23407}, Key = {fds332674} } @article{fds332675, Author = {Gesquiere, LR and Pugh, M and Alberts, SC and Markham, AC}, Title = {Estimation of energetic condition in wild baboons using fecal thyroid hormone determination.}, Journal = {General and comparative endocrinology}, Volume = {260}, Pages = {9-17}, Year = {2018}, Month = {May}, url = {http://dx.doi.org/10.1016/j.ygcen.2018.02.004}, Abstract = {Understanding how environmental and social factors affect reproduction through variation in energetic condition remains understudied in wild animals, in large part because accurately and repeatedly measuring energetic condition in the wild is a challenge. Thyroid hormones (THs), such as triiodothyronine (T3) and thyroxine (T4), have a key role in mitigating metabolic responses to energy intake and expenditure, and therefore are considered important biomarkers of an animal's energetic condition. Recent method development has shown that T3 and T4 metabolites can be measured in feces, but studies measuring THs in wild populations remain rare. Here we measured fecal T3 metabolites (mT3) in baboons, and tested whether the conditions of collection and storage used for steroid hormones could also be used for mT3; we focused on mT3 as it is the biologically active form of TH and because fecal T4 metabolites (mT4) were below detection levels in our samples. We also tested if mT3 could be determined in freeze-dried samples stored for long periods of time, and if these concentrations reflected expected biological variations across seasons and reproductive states. Our results show that mT3 can be measured with accuracy and precision in baboon feces. The conditions of collection and storage we use for steroid hormones are appropriate for mT3 determination. In addition, mT3 concentrations can be determined in samples stored at -20 °C for up to 9 years, and are not predicted by the amount of time in storage. As expected, wild female baboons have lower mT3 concentrations during the dry season. Interestingly, mT3 concentrations are lower in pregnant and lactating females, possibly reflecting an energy sparing mechanism. Retroactive determination of mT3 concentration in stored, freeze-dried feces opens the door to novel studies on the role of energetic condition on fitness in wild animals.}, Doi = {10.1016/j.ygcen.2018.02.004}, Key = {fds332675} } @article{fds332676, Author = {Tucker, MA and Böhning-Gaese, K and Fagan, WF and Fryxell, JM and Van Moorter, B and Alberts, SC and Ali, AH and Allen, AM and Attias, N and Avgar, T and Bartlam-Brooks, H and Bayarbaatar, B and Belant, JL and Bertassoni, A and Beyer, D and Bidner, L and van Beest, FM and Blake, S and Blaum, N and Bracis, C and Brown, D and de Bruyn, PJN and Cagnacci, F and Calabrese, JM and Camilo-Alves, C and Chamaillé-Jammes, S and Chiaradia, A and Davidson, SC and Dennis, T and DeStefano, S and Diefenbach, D and Douglas-Hamilton, I and Fennessy, J and Fichtel, C and Fiedler, W and Fischer, C and Fischhoff, I and Fleming, CH and Ford, AT and Fritz, SA and Gehr, B and Goheen, JR and Gurarie, E and Hebblewhite, M and Heurich, M and Hewison, AJM and Hof, C and Hurme, E and Isbell, LA and Janssen, R and Jeltsch, F and Kaczensky, P and Kane, A and Kappeler, PM and Kauffman, M and Kays, R and Kimuyu, D and Koch, F and Kranstauber, B and LaPoint, S and Leimgruber, P and Linnell, JDC and López-López, P and Markham, AC and Mattisson, J and Medici, EP and Mellone, U and Merrill, E and de Miranda Mourão and G and Morato, RG and Morellet, N and Morrison, TA and Díaz-Muñoz, SL and Mysterud, A and Nandintsetseg, D and Nathan, R and Niamir, A and Odden, J and O'Hara, RB and Oliveira-Santos, LGR and Olson, KA and Patterson, BD and Cunha de Paula and R and Pedrotti, L and Reineking, B and Rimmler, M and Rogers, TL and Rolandsen, CM and Rosenberry, CS and Rubenstein, DI and Safi, K and Saïd, S and Sapir, N and Sawyer, H and Schmidt, NM and Selva, N and Sergiel, A and Shiilegdamba, E and Silva, JP and Singh, N and Solberg, EJ and Spiegel, O and Strand, O and Sundaresan, S and Ullmann, W and Voigt, U and Wall, J and Wattles, D and Wikelski, M and Wilmers, CC and Wilson, JW and Wittemyer, G and Zięba, F and Zwijacz-Kozica, T and Mueller, T}, Title = {Moving in the Anthropocene: Global reductions in terrestrial mammalian movements.}, Journal = {Science (New York, N.Y.)}, Volume = {359}, Number = {6374}, Pages = {466-469}, Year = {2018}, Month = {January}, url = {http://dx.doi.org/10.1126/science.aam9712}, Abstract = {Animal movement is fundamental for ecosystem functioning and species survival, yet the effects of the anthropogenic footprint on animal movements have not been estimated across species. Using a unique GPS-tracking database of 803 individuals across 57 species, we found that movements of mammals in areas with a comparatively high human footprint were on average one-half to one-third the extent of their movements in areas with a low human footprint. We attribute this reduction to behavioral changes of individual animals and to the exclusion of species with long-range movements from areas with higher human impact. Global loss of vagility alters a key ecological trait of animals that affects not only population persistence but also ecosystem processes such as predator-prey interactions, nutrient cycling, and disease transmission.}, Doi = {10.1126/science.aam9712}, Key = {fds332676} } @article{fds335220, Author = {Lea, A and Akinyi, M and Nyakundi, R and Mareri, P and Nyundo, F and Kariuki, T and Alberts, S and Archie, E and Tung, J}, Title = {Dominance rank-associated immune gene expression is widespread, sex-specific, and a precursor to high social status in wild male baboons}, Year = {2018}, url = {http://dx.doi.org/10.1101/366021}, Abstract = {<h4>ABSTRACT</h4> In humans and other hierarchical species, social status is tightly linked to variation in health and fitness-related traits. Experimental manipulations of social status in female rhesus macaques suggest that this relationship is partially explained by status effects on immune gene regulation. However, social hierarchies are established and maintained in different ways across species: while some are based on kin-directed nepotism, others emerge from direct physical competition. We investigated how this variation influences the relationship between social status and immune gene regulation in wild baboons, where hierarchies in males are based on fighting ability but female hierarchies are nepotistic. We measured rank-related variation in gene expression levels in adult baboons of both sexes at baseline and in response to ex vivo stimulation with the bacterial endotoxin lipopolysaccharide (LPS). We identified >2000 rank- associated genes in males, an order of magnitude more than in females. In males, high status predicted increased expression of genes involved in innate immunity and preferential activation of the NFkB-mediated pro-inflammatory pathway, a pattern previously associated with low status in female rhesus macaques. Using Mendelian randomization, we reconcile these observations by demonstrating that high status-associated gene expression patterns are precursors, not consequences, of high social status in males, in support of the idea that physiological condition determines who attains high rank. Together, our work provides the first test of the relationship between social status and immune gene regulation in wild primates. It also emphasizes the importance of social context in shaping the relationship between social status and immune function. <h4>SIGNIFICANCE</h4> Social status predicts fitness outcomes in social animals, motivating efforts to understand its physiological causes and consequences. We investigated the relationship between social status and immune gene expression in wild baboons, where female status is determined by kinship but male status is determined by fighting ability. We uncover pervasive status-gene expression associations in males, but not females. High status males exhibit high levels of pro-inflammatory gene expression, in contrast to previous findings in hierarchies that are not competitively determined. Using Mendelian randomization, we show that this status-associated variation precedes dominance rank attainment: males who compete successfully for high status are already immunologically distinct. The nature of social hierarchies thus fundamentally shapes the relationship between social status and immune function.}, Doi = {10.1101/366021}, Key = {fds335220} } @article{fds326807, Author = {Campos, FA and Morris, WF and Alberts, SC and Altmann, J and Brockman, DK and Cords, M and Pusey, A and Stoinski, TS and Strier, KB and Fedigan, LM}, Title = {Does climate variability influence the demography of wild primates? Evidence from long-term life-history data in seven species.}, Journal = {Global change biology}, Volume = {23}, Number = {11}, Pages = {4907-4921}, Year = {2017}, Month = {November}, url = {http://dx.doi.org/10.1111/gcb.13754}, Abstract = {Earth's rapidly changing climate creates a growing need to understand how demographic processes in natural populations are affected by climate variability, particularly among organisms threatened by extinction. Long-term, large-scale, and cross-taxon studies of vital rate variation in relation to climate variability can be particularly valuable because they can reveal environmental drivers that affect multiple species over extensive regions. Few such data exist for animals with slow life histories, particularly in the tropics, where climate variation over large-scale space is asynchronous. As our closest relatives, nonhuman primates are especially valuable as a resource to understand the roles of climate variability and climate change in human evolutionary history. Here, we provide the first comprehensive investigation of vital rate variation in relation to climate variability among wild primates. We ask whether primates are sensitive to global changes that are universal (e.g., higher temperature, large-scale climate oscillations) or whether they are more sensitive to global change effects that are local (e.g., more rain in some places), which would complicate predictions of how primates in general will respond to climate change. To address these questions, we use a database of long-term life-history data for natural populations of seven primate species that have been studied for 29-52 years to investigate associations between vital rate variation, local climate variability, and global climate oscillations. Associations between vital rates and climate variability varied among species and depended on the time windows considered, highlighting the importance of temporal scale in detection of such effects. We found strong climate signals in the fertility rates of three species. However, survival, which has a greater impact on population growth, was little affected by climate variability. Thus, we found evidence for demographic buffering of life histories, but also evidence of mechanisms by which climate change could affect the fates of wild primates.}, Doi = {10.1111/gcb.13754}, Key = {fds326807} } @article{fds331196, Author = {Grieneisen, LE and Livermore, J and Alberts, S and Tung, J and Archie, EA}, Title = {Group Living and Male Dispersal Predict the Core Gut Microbiome in Wild Baboons.}, Journal = {Integrative and comparative biology}, Volume = {57}, Number = {4}, Pages = {770-785}, Year = {2017}, Month = {October}, url = {http://dx.doi.org/10.1093/icb/icx046}, Abstract = {The mammalian gut microbiome plays a profound role in the physiology, metabolism, and overall health of its host. However, biologists have only a nascent understanding of the forces that drive inter-individual heterogeneity in gut microbial composition, especially the role of host social environment. Here we used 178 samples from 78 wild yellow baboons (Papio cynocephalus) living in two social groups to test how host social context, including group living, social interactions within groups, and transfer between social groups (e.g., dispersal) predict inter-individual variation in gut microbial alpha and beta diversity. We also tested whether social effects differed for prevalent "core" gut microbial taxa, which are thought to provide primary functions to hosts, versus rare "non-core" microbes, which may represent relatively transient environmental acquisitions. Confirming prior studies, we found that each social group harbored a distinct gut microbial community. These differences included both non-core and core gut microbial taxa, suggesting that these effects are not solely driven by recent gut microbial exposures. Within social groups, close grooming partners had more similar core microbiomes, but not non-core microbiomes, than individuals who rarely groomed each other, even controlling for kinship and diet similarity between grooming partners. Finally, in support of the idea that the gut microbiome can be altered by current social context, we found that the longer an immigrant male had lived in a given social group, the more closely his gut microbiome resembled the gut microbiomes of the group's long-term residents. Together, these results reveal the importance of a host's social context in shaping the gut microbiome and shed new light onto the microbiome-related consequences of male dispersal.}, Doi = {10.1093/icb/icx046}, Key = {fds331196} } @article{fds328092, Author = {Akinyi, MY and Gesquiere, LR and Franz, M and Onyango, PO and Altmann, J and Alberts, SC}, Title = {Hormonal correlates of natal dispersal and rank attainment in wild male baboons.}, Journal = {Hormones and behavior}, Volume = {94}, Pages = {153-161}, Year = {2017}, Month = {August}, url = {http://dx.doi.org/10.1016/j.yhbeh.2017.07.005}, Abstract = {In many mammals, maturational milestones such as dispersal and the attainment of adult dominance rank mark stages in the onset of reproductive activity and depend on a coordinated set of hormonal and socio-behavioral changes. Studies that focus on the link between hormones and maturational milestones are uncommon in wild mammals because of the challenges of obtaining adequate sample sizes of maturing animals and of tracking the movements of dispersing animals. We examined two maturational milestones in wild male baboons-adult dominance rank attainment and natal dispersal-and measured their association with variation in glucocorticoids (fGC) and fecal testosterone (fT). We found that rank attainment is associated with an increase in fGC levels but not fT levels: males that have achieved any adult rank have higher fGC than males that have not yet attained an adult rank. This indicates that once males have attained an adult rank they experience greater energetic and/or psychosocial demands than they did prior to attaining this milestone, most likely because of the resulting participation in both agonistic and sexual behaviors that accompany rank attainment. In contrast, natal dispersal does not produce sustained increases in either fGC or fT levels, suggesting that individuals are either well adapted to face the challenges associated with dispersal or that the effects of dispersal on hormone levels are ephemeral for male baboons.}, Doi = {10.1016/j.yhbeh.2017.07.005}, Key = {fds328092} } @article{fds325577, Author = {Miller, EA and Livermore, JA and Alberts, SC and Tung, J and Archie, EA}, Title = {Ovarian cycling and reproductive state shape the vaginal microbiota in wild baboons.}, Journal = {Microbiome}, Volume = {5}, Number = {1}, Pages = {8}, Year = {2017}, Month = {January}, url = {http://dx.doi.org/10.1186/s40168-017-0228-z}, Abstract = {<h4>Background</h4>The vaginal microbiome is an important site of bacterial-mammalian symbiosis. This symbiosis is currently best characterized for humans, where lactobacilli dominate the microbial community and may help defend women against infectious disease. However, lactobacilli do not dominate the vaginal microbiota of any other mammal studied to date, raising key questions about the forces that shape the vaginal microbiome in non-human mammals.<h4>Results</h4>We used Illumina sequencing of the bacterial 16S rRNA gene to investigate variation in the taxonomic composition of the vaginal microbiota in 48 baboons (Papio cynocephalus), members of a well-studied wild population in Kenya. Similar to prior studies, we found that the baboon vaginal microbiota was not dominated by lactobacilli. Despite this difference, and similar to humans, reproductive state was the dominant predictor of baboon vaginal microbiota, with pregnancy, postpartum amenorrhea, and ovarian cycling explaining 18% of the variance in community composition. Furthermore, among cycling females, a striking 39% of variance in community composition was explained by ovarian cycle phase, with an especially distinctive microbial community around ovulation. Periovulatory females exhibited the highest relative abundance of lactic acid-producing bacteria compared to any other phase, with a mean relative abundance of 44%. To a lesser extent, sexual behavior, especially a history of shared sexual partners, also predicted vaginal microbial similarity between baboons.<h4>Conclusions</h4>Despite striking differences in their dominant microbes, both human and baboon vaginal microbiota exhibit profound changes in composition in response to reproductive state, ovarian cycle phase, and sexual behavior. We found major shifts in composition during ovulation, which may have implications for disease risk and conception success. These findings highlight the need for future studies to account for fine-scale differences in reproductive state, particularly differences between the various phases of the ovarian cycle. Overall, our work contributes to an emerging understanding of the forces that explain intra- and inter-individual variation in the mammalian vaginal microbiome, with particular emphasis on its role in host health and disease risk.}, Doi = {10.1186/s40168-017-0228-z}, Key = {fds325577} } @article{fds335221, Author = {Lea, AJ and Tung, J and Archie, EA and Alberts, SC}, Title = {Developmental plasticity: Bridging research in evolution and human health.}, Journal = {Evolution, medicine, and public health}, Volume = {2017}, Number = {1}, Pages = {162-175}, Year = {2017}, Month = {January}, url = {http://dx.doi.org/10.1093/emph/eox019}, Abstract = {Early life experiences can have profound and persistent effects on traits expressed throughout the life course, with consequences for later life behavior, disease risk, and mortality rates. The shaping of later life traits by early life environments, known as 'developmental plasticity', has been well-documented in humans and non-human animals, and has consequently captured the attention of both evolutionary biologists and researchers studying human health. Importantly, the parallel significance of developmental plasticity across multiple fields presents a timely opportunity to build a comprehensive understanding of this phenomenon. We aim to facilitate this goal by highlighting key outstanding questions shared by both evolutionary and health researchers, and by identifying theory and empirical work from both research traditions that is designed to address these questions. Specifically, we focus on: (i) evolutionary explanations for developmental plasticity, (ii) the genetics of developmental plasticity and (iii) the molecular mechanisms that mediate developmental plasticity. In each section, we emphasize the conceptual gains in human health and evolutionary biology that would follow from filling current knowledge gaps using interdisciplinary approaches. We encourage researchers interested in developmental plasticity to evaluate their own work in light of research from diverse fields, with the ultimate goal of establishing a cross-disciplinary understanding of developmental plasticity.}, Doi = {10.1093/emph/eox019}, Key = {fds335221} } @article{fds335222, Author = {Lea, AJ and Tung, J and Archie, EA and Alberts, SC}, Title = {Developmental plasticity research in evolution and human health: Response to commentaries.}, Journal = {Evolution, medicine, and public health}, Volume = {2017}, Number = {1}, Pages = {201-205}, Year = {2017}, Month = {January}, url = {http://dx.doi.org/10.1093/emph/eoy007}, Doi = {10.1093/emph/eoy007}, Key = {fds335222} } @article{fds324017, Author = {Zipple, MN and Grady, JH and Gordon, JB and Chow, LD and Archie, EA and Altmann, J and Alberts, SC}, Title = {Conditional fetal and infant killing by male baboons.}, Journal = {Proceedings. Biological sciences}, Volume = {284}, Number = {1847}, Pages = {20162561}, Year = {2017}, Month = {January}, url = {http://dx.doi.org/10.1098/rspb.2016.2561}, Abstract = {Sexually selected feticide-the death of infants in utero as a result of male behaviour-has only rarely been described or analysed, although it is presumed to be favoured by the same selective pressures that favour sexually selected infanticide. To test this hypothesis, we measured the frequency of feticide and infanticide by male baboons of the Amboseli basin in Kenya, and examined which characteristics of a male and his environment made him more likely to commit feticide and/or infanticide. We found a dramatic increase in fetal and infant death rates, but no increase in death rates of 1- to 2-year-old individuals, following the immigration of males who stood to benefit from feticide and infanticide. Specifically, fetal and infant death rates were highest following immigrations in which: (i) the immigrant male rapidly attained high rank, (ii) that male remained consistently resident in the group for at least three months, (iii) food availability and social group range overlap was relatively low and (iv) relatively many pregnant females and/or dependent infants were present. Together, these results provide strong evidence for the existence of both sexually selected feticide and infanticide in our population, and they indicate that feticide and infanticide are conditional male behavioural strategies employed under particular circumstances.}, Doi = {10.1098/rspb.2016.2561}, Key = {fds324017} } @article{fds321554, Author = {Colchero, F and Rau, R and Jones, OR and Barthold, JA and Conde, DA and Lenart, A and Nemeth, L and Scheuerlein, A and Schoeley, J and Torres, C and Zarulli, V and Altmann, J and Brockman, DK and Bronikowski, AM and Fedigan, LM and Pusey, AE and Stoinski, TS and Strier, KB and Baudisch, A and Alberts, SC and Vaupel, JW}, Title = {The emergence of longevous populations.}, Journal = {Proceedings of the National Academy of Sciences of the United States of America}, Volume = {113}, Number = {48}, Pages = {E7681-E7690}, Year = {2016}, Month = {November}, url = {http://dx.doi.org/10.1073/pnas.1612191113}, Abstract = {The human lifespan has traversed a long evolutionary and historical path, from short-lived primate ancestors to contemporary Japan, Sweden, and other longevity frontrunners. Analyzing this trajectory is crucial for understanding biological and sociocultural processes that determine the span of life. Here we reveal a fundamental regularity. Two straight lines describe the joint rise of life expectancy and lifespan equality: one for primates and the second one over the full range of human experience from average lifespans as low as 2 y during mortality crises to more than 87 y for Japanese women today. Across the primate order and across human populations, the lives of females tend to be longer and less variable than the lives of males, suggesting deep evolutionary roots to the male disadvantage. Our findings cast fresh light on primate evolution and human history, opening directions for research on inequality, sociality, and aging.}, Doi = {10.1073/pnas.1612191113}, Key = {fds321554} } @article{fds318015, Author = {Wall, JD and Schlebusch, SA and Alberts, SC and Cox, LA and Snyder-Mackler, N and Nevonen, KA and Carbone, L and Tung, J}, Title = {Genomewide ancestry and divergence patterns from low-coverage sequencing data reveal a complex history of admixture in wild baboons.}, Journal = {Molecular ecology}, Volume = {25}, Number = {14}, Pages = {3469-3483}, Year = {2016}, Month = {July}, url = {http://dx.doi.org/10.1111/mec.13684}, Abstract = {Naturally occurring admixture has now been documented in every major primate lineage, suggesting its key role in primate evolutionary history. Active primate hybrid zones can provide valuable insight into this process. Here, we investigate the history of admixture in one of the best-studied natural primate hybrid zones, between yellow baboons (Papio cynocephalus) and anubis baboons (Papio anubis) in the Amboseli ecosystem of Kenya. We generated a new genome assembly for yellow baboon and low-coverage genomewide resequencing data from yellow baboons, anubis baboons and known hybrids (n = 44). Using a novel composite likelihood method for estimating local ancestry from low-coverage data, we found high levels of genetic diversity and genetic differentiation between the parent taxa, and excellent agreement between genome-scale ancestry estimates and a priori pedigree, life history and morphology-based estimates (r(2) = 0.899). However, even putatively unadmixed Amboseli yellow individuals carried a substantial proportion of anubis ancestry, presumably due to historical admixture. Further, the distribution of shared vs. fixed differences between a putatively unadmixed Amboseli yellow baboon and an unadmixed anubis baboon, both sequenced at high coverage, is inconsistent with simple isolation-migration or equilibrium migration models. Our findings suggest a complex process of intermittent contact that has occurred multiple times in baboon evolutionary history, despite no obvious fitness costs to hybrids or major geographic or behavioural barriers. In combination with the extensive phenotypic data available for baboon hybrids, our results provide valuable context for understanding the history of admixture in primates, including in our own lineage.}, Doi = {10.1111/mec.13684}, Key = {fds318015} } @article{fds318016, Author = {Snyder-Mackler, N and Majoros, WH and Yuan, ML and Shaver, AO and Gordon, JB and Kopp, GH and Schlebusch, SA and Wall, JD and Alberts, SC and Mukherjee, S and Zhou, X and Tung, J}, Title = {Efficient Genome-Wide Sequencing and Low-Coverage Pedigree Analysis from Noninvasively Collected Samples.}, Journal = {Genetics}, Volume = {203}, Number = {2}, Pages = {699-714}, Year = {2016}, Month = {June}, url = {http://dx.doi.org/10.1534/genetics.116.187492}, Abstract = {Research on the genetics of natural populations was revolutionized in the 1990s by methods for genotyping noninvasively collected samples. However, these methods have remained largely unchanged for the past 20 years and lag far behind the genomics era. To close this gap, here we report an optimized laboratory protocol for genome-wide capture of endogenous DNA from noninvasively collected samples, coupled with a novel computational approach to reconstruct pedigree links from the resulting low-coverage data. We validated both methods using fecal samples from 62 wild baboons, including 48 from an independently constructed extended pedigree. We enriched fecal-derived DNA samples up to 40-fold for endogenous baboon DNA and reconstructed near-perfect pedigree relationships even with extremely low-coverage sequencing. We anticipate that these methods will be broadly applicable to the many research systems for which only noninvasive samples are available. The lab protocol and software ("WHODAD") are freely available at www.tung-lab.org/protocols-and-software.html and www.xzlab.org/software.html, respectively.}, Doi = {10.1534/genetics.116.187492}, Key = {fds318016} } @article{fds227746, Author = {Ren, T and Grieneisen, LE and Alberts, SC and Archie, EA and Wu, M}, Title = {Development, diet and dynamism: longitudinal and cross-sectional predictors of gut microbial communities in wild baboons.}, Journal = {Environmental microbiology}, Volume = {18}, Number = {5}, Pages = {1312-1325}, Year = {2016}, Month = {May}, ISSN = {1462-2912}, url = {http://dx.doi.org/10.1111/1462-2920.12852}, Abstract = {Gut bacterial communities play essential roles in host biology, but to date we lack information on the forces that shape gut microbiota between hosts and over time in natural populations. Understanding these forces in wild primates provides a valuable comparative context that enriches scientific perspectives on human gut microbiota. To this end, we tested predictors of gut microbial composition in a well-studied population of wild baboons. Using cross-sectional and longitudinal samples collected over 13 years, we found that baboons harbour gut microbiota typical of other omnivorous primates, albeit with an especially high abundance of Bifidobacterium. Similar to previous work in humans and other primates, we found strong effects of both developmental transitions and diet on gut microbial composition. Strikingly, baboon gut microbiota appeared to be highly dynamic such that samples collected from the same individual only a few days apart were as different from each other as samples collected over 10 years apart. Despite the dynamic nature of baboon gut microbiota, we identified a set of core taxa that is common among primates, supporting the hypothesis that microbiota codiversify with their host species. Our analysis identified two tentative enterotypes in adult baboons that differ from those of humans and chimpanzees.}, Doi = {10.1111/1462-2920.12852}, Key = {fds227746} } @article{fds314361, Author = {Tung, J and Archie, EA and Altmann, J and Alberts, SC}, Title = {Cumulative early life adversity predicts longevity in wild baboons}, Journal = {Nat Commun}, Volume = {7}, Pages = {11181}, Publisher = {Nature Publishing Group, a division of Macmillan Publishers Limited. All Rights Reserved.}, Year = {2016}, Month = {April}, url = {http://hdl.handle.net/10161/11825 Duke open access}, Abstract = {In humans and other animals, harsh circumstances in early life predict morbidity and mortality in adulthood. Multiple adverse conditions are thought to be especially toxic, but this hypothesis has rarely been tested in a prospective, longitudinal framework, especially in long-lived mammals. Here we use prospective data on 196 wild female baboons to show that cumulative early adversity predicts natural adult lifespan. Females who experience [ge]3 sources of early adversity die a median of 10 years earlier than females who experience [le]1 adverse circumstances (median lifespan is 18.5 years). Females who experience the most adversity are also socially isolated in adulthood, suggesting that social processes partially explain the link between early adversity and adult survival. Our results provide powerful evidence for the developmental origins of health and disease and indicate that close ties between early adversity and survival arise even in the absence of health habit and health care-related explanations.}, Doi = {10.1038/ncomms11181}, Key = {fds314361} } @article{fds227747, Author = {Beehner, JC and Gesquiere, L and Seyfarth, RM and Cheney, DL and Alberts, SC and Altmann, J}, Title = {Corrigendum to "Testosterone related to age and life-history stages in male baboons and geladas" [Horm. Behav. 56/4 (2009) 472-480].}, Journal = {Hormones and behavior}, Volume = {80}, Pages = {149}, Year = {2016}, Month = {April}, ISSN = {0018-506X}, url = {http://dx.doi.org/10.1016/j.yhbeh.2015.08.004}, Doi = {10.1016/j.yhbeh.2015.08.004}, Key = {fds227747} } @article{fds315541, Author = {Lea, AJ and Altmann, J and Alberts, SC and Tung, J}, Title = {Resource base influences genome-wide DNA methylation levels in wild baboons (Papio cynocephalus).}, Journal = {Molecular ecology}, Volume = {25}, Number = {8}, Pages = {1681-1696}, Year = {2016}, Month = {April}, ISSN = {0962-1083}, url = {http://dx.doi.org/10.1111/mec.13436}, Abstract = {Variation in resource availability commonly exerts strong effects on fitness-related traits in wild animals. However, we know little about the molecular mechanisms that mediate these effects, or about their persistence over time. To address these questions, we profiled genome-wide whole-blood DNA methylation levels in two sets of wild baboons: (i) 'wild-feeding' baboons that foraged naturally in a savanna environment and (ii) 'Lodge' baboons that had ready access to spatially concentrated human food scraps, resulting in high feeding efficiency and low daily travel distances. We identified 1014 sites (0.20% of sites tested) that were differentially methylated between wild-feeding and Lodge baboons, providing the first evidence that resource availability shapes the epigenome in a wild mammal. Differentially methylated sites tended to occur in contiguous stretches (i.e., in differentially methylated regions or DMRs), in promoters and enhancers, and near metabolism-related genes, supporting their functional importance in gene regulation. In agreement, reporter assay experiments confirmed that methylation at the largest identified DMR, located in the promoter of a key glycolysis-related gene, was sufficient to causally drive changes in gene expression. Intriguingly, all dispersing males carried a consistent epigenetic signature of their membership in a wild-feeding group, regardless of whether males dispersed into or out of this group as adults. Together, our findings support a role for DNA methylation in mediating ecological effects on phenotypic traits in the wild and emphasize the dynamic environmental sensitivity of DNA methylation levels across the life course.}, Doi = {10.1111/mec.13436}, Key = {fds315541} } @article{fds333004, Author = {Bronikowski, AM and Cords, M and Alberts, SC and Altmann, J and Brockman, DK and Fedigan, LM and Pusey, A and Stoinski, T and Strier, KB and Morris, WF}, Title = {Female and male life tables for seven wild primate species.}, Journal = {Scientific data}, Volume = {3}, Pages = {160006}, Year = {2016}, Month = {March}, url = {http://dx.doi.org/10.1038/sdata.2016.6}, Abstract = {We provide male and female census count data, age-specific survivorship, and female age-specific fertility estimates for populations of seven wild primates that have been continuously monitored for at least 29 years: sifaka (Propithecus verreauxi) in Madagascar; muriqui (Brachyteles hypoxanthus) in Brazil; capuchin (Cebus capucinus) in Costa Rica; baboon (Papio cynocephalus) and blue monkey (Cercopithecus mitis) in Kenya; chimpanzee (Pan troglodytes) in Tanzania; and gorilla (Gorilla beringei) in Rwanda. Using one-year age-class intervals, we computed point estimates of age-specific survival for both sexes. In all species, our survival estimates for the dispersing sex are affected by heavy censoring. We also calculated reproductive value, life expectancy, and mortality hazards for females. We used bootstrapping to place confidence intervals on life-table summary metrics (R0, the net reproductive rate; λ, the population growth rate; and G, the generation time). These data have high potential for reuse; they derive from continuous population monitoring of long-lived organisms and will be invaluable for addressing questions about comparative demography, primate conservation and human evolution.}, Doi = {10.1038/sdata.2016.6}, Key = {fds333004} } @article{fds315540, Author = {Markham, AC and Alberts, SC and Altmann, J}, Title = {Haven for the night: Sleeping site selection in a wild primate}, Journal = {Behavioral Ecology}, Volume = {27}, Number = {1}, Pages = {29-35}, Publisher = {Oxford University Press (OUP)}, Year = {2016}, Month = {January}, ISSN = {1045-2249}, url = {http://dx.doi.org/10.1093/beheco/arv118}, Abstract = {Many animals seek refuge when they sleep, often employing different sleeping sites in successive time periods. Switching from one sleeping site to another might reduce predation or parasite exposure or increase proximity to food resources that are temporally and spatially heterogenous. However, achieving these effects will depend on the synchronous and nonsynchronous use of the same sleeping sites by conspecifics. We assessed the use of multiple sleeping sites by 5 wild baboon (Papio cynocephalus) social groups to evaluate how sites were exploited at both the population and group level. Of 126 woodland sleeping sites used by the study population over ~900 nights of observation, 10 sites were used more than 100 times; these preferred sites accounted for ~60% of all known sleeping sites. On average, individual groups left sleeping sites after 1-2 nights of continuous use, and the same group did not reuse a site for an average of 45 nights. However, at the population level, preferred sites were reused on average every 4 nights. This near-continuous occupation suggests that groups competed for access to preferred sites, perhaps because preferred sites represented better protection from predators, lower parasite prevalence, or had better foraging opportunities nearby. The number of trees in a sleeping site and the time since a site was last used were significant factors distinguishing sites used on a given night by the most dominant versus most subordinate social group. These findings highlight the importance of evaluating resource use at multiple levels of social organization.}, Doi = {10.1093/beheco/arv118}, Key = {fds315540} } @article{fds335223, Author = {Alberts, S}, Title = {The Challenge of Survival for Wild Infant Baboons}, Journal = {American Scientist}, Volume = {104}, Number = {6}, Pages = {366-366}, Publisher = {Sigma Xi}, Year = {2016}, url = {http://dx.doi.org/10.1511/2016.123.366}, Doi = {10.1511/2016.123.366}, Key = {fds335223} } @article{fds329881, Author = {Markham, AC and Gesquiere, LR and Alberts, SC and Altmann, J}, Title = {Optimal group size in a highly social mammal.}, Journal = {Proceedings of the National Academy of Sciences of the United States of America}, Volume = {112}, Number = {48}, Pages = {14882-14887}, Year = {2015}, Month = {December}, url = {http://dx.doi.org/10.1073/pnas.1517794112}, Abstract = {Group size is an important trait of social animals, affecting how individuals allocate time and use space, and influencing both an individual's fitness and the collective, cooperative behaviors of the group as a whole. Here we tested predictions motivated by the ecological constraints model of group size, examining the effects of group size on ranging patterns and adult female glucocorticoid (stress hormone) concentrations in five social groups of wild baboons (Papio cynocephalus) over an 11-y period. Strikingly, we found evidence that intermediate-sized groups have energetically optimal space-use strategies; both large and small groups experience ranging disadvantages, in contrast to the commonly reported positive linear relationship between group size and home range area and daily travel distance, which depict a disadvantage only in large groups. Specifically, we observed a U-shaped relationship between group size and home range area, average daily distance traveled, evenness of space use within the home range, and glucocorticoid concentrations. We propose that a likely explanation for these U-shaped patterns is that large, socially dominant groups are constrained by within-group competition, whereas small, socially subordinate groups are constrained by between-group competition and predation pressures. Overall, our results provide testable hypotheses for evaluating group-size constraints in other group-living species, in which the costs of intra- and intergroup competition vary as a function of group size.}, Doi = {10.1073/pnas.1517794112}, Key = {fds329881} } @article{fds314312, Author = {Franz, M and Alberts, SC}, Title = {Social network dynamics: the importance of distinguishing between heterogeneous and homogeneous changes.}, Journal = {Behavioral ecology and sociobiology}, Volume = {69}, Number = {12}, Pages = {2059-2069}, Year = {2015}, Month = {December}, ISSN = {0340-5443}, url = {http://dx.doi.org/10.1007/s00265-015-2030-x}, Abstract = {Social network analysis is increasingly applied to understand the evolution of animal sociality. Identifying ecological and evolutionary drivers of complex social structures requires inferring how social networks change over time. In most observational studies, sampling errors may affect the apparent network structures.Here, we argue that existing approaches tend not to control sufficiently for some types of sampling errors when social networks change over time. Specifically, we argue that two different types of changes may occur in social networks, heterogeneous and homogeneous changes, and that understanding network dynamics requires distinguishing between these two different types of changes, which are not mutually exclusive. Heterogeneous changes occur if relationships change differentially, e.g. if some relationships are terminated but others remain intact. Homogeneous changes occur if all relationships are proportionally affected in the same way, e.g. if grooming rates decline similarly across all dyads. Homogeneous declines in the strength of relationships can strongly reduce the probability of observing weak relationships, producing the appearance of heterogeneous network changes. Using simulations, we confirm that failing to differentiate homogeneous and heterogeneous changes can potentially lead to false conclusions about network dynamics. We also show that bootstrap tests fail to distinguish between homogeneous and heterogeneous changes. As a solution to this problem we show that an appropriate randomization test can infer whether heterogeneous changes occurred. Finally, we illustrate the utility of using the randomization test by performing an example analysis using an empirical data set on wild baboons.}, Doi = {10.1007/s00265-015-2030-x}, Key = {fds314312} } @article{fds314311, Author = {Franz, M and McLean, E and Tung, J and Altmann, J and Alberts, SC}, Title = {Self-organizing dominance hierarchies in a wild primate population.}, Journal = {Proceedings. Biological sciences}, Volume = {282}, Number = {1814}, Pages = {20151512}, Year = {2015}, Month = {September}, ISSN = {0962-8452}, url = {http://dx.doi.org/10.1098/rspb.2015.1512}, Abstract = {Linear dominance hierarchies, which are common in social animals, can profoundly influence access to limited resources, reproductive opportunities and health. In spite of their importance, the mechanisms that govern the dynamics of such hierarchies remain unclear. Two hypotheses explain how linear hierarchies might emerge and change over time. The 'prior attributes hypothesis' posits that individual differences in fighting ability directly determine dominance ranks. By contrast, the 'social dynamics hypothesis' posits that dominance ranks emerge from social self-organization dynamics such as winner and loser effects. While the prior attributes hypothesis is well supported in the literature, current support for the social dynamics hypothesis is limited to experimental studies that artificially eliminate or minimize individual differences in fighting abilities. Here, we present the first evidence supporting the social dynamics hypothesis in a wild population. Specifically, we test for winner and loser effects on male hierarchy dynamics in wild baboons, using a novel statistical approach based on the Elo rating method for cardinal rank assignment, which enables the detection of winner and loser effects in uncontrolled group settings. Our results demonstrate (i) the presence of winner and loser effects, and (ii) that individual susceptibility to such effects may have a genetic basis. Taken together, our results show that both social self-organization dynamics and prior attributes can combine to influence hierarchy dynamics even when agonistic interactions are strongly influenced by differences in individual attributes. We hypothesize that, despite variation in individual attributes, winner and loser effects exist (i) because these effects could be particularly beneficial when fighting abilities in other group members change over time, and (ii) because the coevolution of prior attributes and winner and loser effects maintains a balance of both effects.}, Doi = {10.1098/rspb.2015.1512}, Key = {fds314311} } @article{fds227748, Author = {Nunn, CL and Alberts, SC and McClain, CR and Meshnick, SR and Vision, TJ and Wiegmann, BM and Rodrigo, AG}, Title = {Linking Evolution, Ecology, and Health: TriCEM}, Journal = {BioScience}, Volume = {65}, Number = {8}, Pages = {748-749}, Publisher = {Oxford University Press (OUP)}, Year = {2015}, Month = {July}, ISSN = {0006-3568}, url = {http://dx.doi.org/10.1093/biosci/biv086}, Doi = {10.1093/biosci/biv086}, Key = {fds227748} } @article{fds227749, Author = {Fitzpatrick, CL and Altmann, J and Alberts, SC}, Title = {Exaggerated sexual swellings and male mate choice in primates: testing the reliable indicator hypothesis in the Amboseli baboons.}, Journal = {Animal behaviour}, Volume = {104}, Pages = {175-185}, Year = {2015}, Month = {June}, ISSN = {0003-3472}, url = {http://dx.doi.org/10.1016/j.anbehav.2015.03.019}, Abstract = {The paradigm of competitive males vying to influence female mate choice has been repeatedly upheld, but, increasingly, studies also report competitive females and choosy males. One female trait that is commonly proposed to influence male mate choice is the exaggerated sexual swelling displayed by females of many Old World primate species. The reliable indicator hypothesis posits that females use the exaggerated swellings to compete for access to mates, and that the swellings advertise variation in female fitness. We tested the two main predictions of this hypothesis in a wild population of baboons (<i>Papio cynocephalus)</i>. First, we examined the effect of swelling size on the probability of mate-guarding ('consortship') by the highest-ranking male and the behavior of those males that trailed consorshipts ('follower males'). Second, we asked whether a female's swelling size predicted several fitness measures. We found that high-ranking males do not prefer females with larger swellings (when controlling for cycle number and conception) and that females with larger swellings did not have higher reproductive success. Our study-the only complete test of the reliable indicator hypothesis in a primate population-rejects the idea that female baboons compete for mates by advertising heritable fitness differences. Furthermore, we found unambiguous evidence that males biased their mating decisions in favor of females who had experienced more sexual cycles since their most recent pregnancy. Thus, rather than tracking the potential differences in fitness between females, male baboons appear to track and target the potential for a given reproductive opportunity to result in fertilization.}, Doi = {10.1016/j.anbehav.2015.03.019}, Key = {fds227749} } @article{fds318017, Author = {Lea, AJ and Altmann, J and Alberts, SC and Tung, J}, Title = {Developmental constraints in a wild primate.}, Journal = {The American naturalist}, Volume = {185}, Number = {6}, Pages = {809-821}, Year = {2015}, Month = {June}, url = {http://dx.doi.org/10.1086/681016}, Abstract = {Early-life experiences can dramatically affect adult traits. However, the evolutionary origins of such early-life effects are debated. The predictive adaptive response hypothesis argues that adverse early environments prompt adaptive phenotypic adjustments that prepare animals for similar challenges in adulthood. In contrast, the developmental constraints hypothesis argues that early adversity is generally costly. To differentiate between these hypotheses, we studied two sets of wild female baboons: those born during low-rainfall, low-quality years and those born during normal-rainfall, high-quality years. For each female, we measured fertility-related fitness components during years in adulthood that matched and mismatched her early conditions. We found support for the developmental constraints hypothesis: females born in low-quality environments showed greater decreases in fertility during drought years than females born in high-quality environments, even though drought years matched the early conditions of females born in low-quality environments. Additionally, we found that females born in low-quality years to high-status mothers did not experience reduced fertility during drought years. These results indicate that early ecological adversity did not prepare individuals to cope with ecological challenges in later life. Instead, individuals that experienced at least one high-quality early environment--either ecological or social--were more resilient to ecological stress in later life. Together, these data suggest that early adversity carries lifelong costs, which is consistent with the developmental constraints hypothesis.}, Doi = {10.1086/681016}, Key = {fds318017} } @article{fds227753, Author = {Tung, J and Barreiro, LB and Burns, MB and Grenier, J-C and Lynch, J and Grieneisen, LE and Altmann, J and Alberts, SC and Blekhman, R and Archie, EA}, Title = {Social networks predict gut microbiome composition in wild baboons.}, Journal = {eLife}, Volume = {4}, Year = {2015}, Month = {March}, url = {http://dx.doi.org/10.7554/elife.05224}, Abstract = {Social relationships have profound effects on health in humans and other primates, but the mechanisms that explain this relationship are not well understood. Using shotgun metagenomic data from wild baboons, we found that social group membership and social network relationships predicted both the taxonomic structure of the gut microbiome and the structure of genes encoded by gut microbial species. Rates of interaction directly explained variation in the gut microbiome, even after controlling for diet, kinship, and shared environments. They therefore strongly implicate direct physical contact among social partners in the transmission of gut microbial species. We identified 51 socially structured taxa, which were significantly enriched for anaerobic and non-spore-forming lifestyles. Our results argue that social interactions are an important determinant of gut microbiome composition in natural animal populations-a relationship with important ramifications for understanding how social relationships influence health, as well as the evolution of group living.}, Doi = {10.7554/elife.05224}, Key = {fds227753} } @article{fds227752, Author = {Tung, J and Zhou, X and Alberts, SC and Stephens, M and Gilad, Y}, Title = {The genetic architecture of gene expression levels in wild baboons.}, Journal = {eLife}, Volume = {4}, Year = {2015}, Month = {February}, url = {http://dx.doi.org/10.7554/elife.04729}, Abstract = {Primate evolution has been argued to result, in part, from changes in how genes are regulated. However, we still know little about gene regulation in natural primate populations. We conducted an RNA sequencing (RNA-seq)-based study of baboons from an intensively studied wild population. We performed complementary expression quantitative trait locus (eQTL) mapping and allele-specific expression analyses, discovering substantial evidence for, and surprising power to detect, genetic effects on gene expression levels in the baboons. eQTL were most likely to be identified for lineage-specific, rapidly evolving genes; interestingly, genes with eQTL significantly overlapped between baboons and a comparable human eQTL data set. Our results suggest that genes vary in their tolerance of genetic perturbation, and that this property may be conserved across species. Further, they establish the feasibility of eQTL mapping using RNA-seq data alone, and represent an important step towards understanding the genetic architecture of gene expression in primates.}, Doi = {10.7554/elife.04729}, Key = {fds227752} } @article{fds227751, Author = {Galbany, J and Tung, J and Altmann, J and Alberts, SC}, Title = {Canine length in wild male baboons: maturation, aging and social dominance rank.}, Journal = {PloS one}, Volume = {10}, Number = {5}, Pages = {e0126415}, Year = {2015}, Month = {January}, url = {http://dx.doi.org/10.1371/journal.pone.0126415}, Abstract = {Canines represent an essential component of the dentition for any heterodont mammal. In primates, like many other mammals, canines are frequently used as weapons. Hence, tooth size and wear may have significant implications for fighting ability, and consequently for social dominance rank, reproductive success, and fitness. We evaluated sources of variance in canine growth and length in a well-studied wild primate population because of the potential importance of canines for male reproductive success in many primates. Specifically, we measured maxillary canine length in 80 wild male baboons (aged 5.04-20.45 years) from the Amboseli ecosystem in southern Kenya, and examined its relationship with maturation, age, and social dominance rank. In our analysis of maturation, we compared food-enhanced baboons (those that fed part time at a refuse pit associated with a tourist lodge) with wild-feeding males, and found that food-enhanced males achieved long canines earlier than wild-feeding males. Among adult males, canine length decreased with age because of tooth wear. We found some evidence that, after controlling for age, longer canines were associated with higher adult dominance rank (accounting for 9% of the variance in rank), but only among relatively high-ranking males. This result supports the idea that social rank, and thus reproductive success and fitness, may depend in part on fighting ability mediated by canine size.}, Doi = {10.1371/journal.pone.0126415}, Key = {fds227751} } @article{fds227754, Author = {Franz, M and Altmann, J and Alberts, SC}, Title = {Knockouts of high-ranking males have limited impact on baboon social networks.}, Journal = {Current zoology}, Volume = {61}, Number = {1}, Pages = {107-113}, Year = {2015}, Month = {January}, ISSN = {1674-5507}, url = {http://dx.doi.org/10.1093/czoolo/61.1.107}, Abstract = {Social network structures can crucially impact complex social processes such as collective behaviour or the transmission of information and diseases. However, currently it is poorly understood how social networks change over time. Previous studies on primates suggest that `knockouts' (due to death or dispersal) of high-ranking individuals might be important drivers for structural changes in animal social networks. Here we test this hypothesis using long-term data on a natural population of baboons, examining the effects of 29 natural knockouts of alpha or beta males on adult female social networks. We investigated whether and how knockouts affected (1) changes in grooming and association rates among adult females, and (2) changes in mean degree and global clustering coefficient in these networks. The only significant effect that we found was a decrease in mean degree in grooming networks in the first month after knockouts, but this decrease was rather small, and grooming networks rebounded to baseline levels by the second month after knockouts. Taken together our results indicate that the removal of high-ranking males has only limited or no lasting effects on social networks of adult female baboons. This finding calls into question the hypothesis that the removal of high-ranking individuals has a destabilizing effect on social network structures in social animals.}, Doi = {10.1093/czoolo/61.1.107}, Key = {fds227754} } @article{fds227757, Author = {Snyder-Mackler, N and Alberts, SC and Bergman, TJ}, Title = {The socio-genetics of a complex society: female gelada relatedness patterns mirror association patterns in a multilevel society.}, Journal = {Molecular ecology}, Volume = {23}, Number = {24}, Pages = {6179-6191}, Year = {2014}, Month = {December}, ISSN = {0962-1083}, url = {http://dx.doi.org/10.1111/mec.12987}, Abstract = {Multilevel societies with fission-fusion dynamics--arguably the most complex animal societies--are defined by two or more nested levels of organization. The core of these societies are modular social units that regularly fission and fuse with one another. Despite convergent evolution in disparate taxa, we know strikingly little about how such societies form and how fitness benefits operate. Understanding the kinship structure of complex societies could inform us about the origins of the social structure as well as about the potential for individuals in these societies to accrue indirect fitness benefits. Here, we combined genetic and behavioural data on geladas (Theropithecus gelada), an Old World Monkey, to complete the most comprehensive socio-genetic analysis of a multilevel society to date. In geladas, individuals in the core social 'units', associate at different frequencies to form 'teams', 'bands' and, the largest aggregations, 'communities'. Units were composed of closely related females, and females remained with their close kin during permanent fissions of units. Interestingly, female-female relatedness also significantly predicted between-unit, between-team and between-band association patterns, while male-male relatedness did not. Thus, it is likely that the socio-genetic structure of gelada society results from females maintaining associations with their female relatives during successive unit fissions--possibly in an attempt to balance the direct and indirect fitness benefits of group living. Overall, the persistence of associations among related females across generations appears to drive the formation of higher levels of gelada society, suggesting that females seek kin for inclusive fitness benefits at multiple levels of gelada society.}, Doi = {10.1111/mec.12987}, Key = {fds227757} } @article{fds227758, Author = {Patzelt, A and Kopp, GH and Ndao, I and Kalbitzer, U and Zinner, D and Fischer, J}, Title = {Male tolerance and male-male bonds in a multilevel primate society.}, Journal = {Proceedings of the National Academy of Sciences of the United States of America}, Volume = {111}, Number = {41}, Pages = {14740-14745}, Year = {2014}, Month = {October}, ISSN = {0027-8424}, url = {http://dx.doi.org/10.1073/pnas.1405811111}, Abstract = {Male relationships in most species of mammals generally are characterized by intense intrasexual competition, with little bonding among unrelated individuals. In contrast, human societies are characterized by high levels of cooperation and strong bonds among both related and unrelated males. The emergence of cooperative male-male relationships has been linked to the multilevel structure of traditional human societies. Based on an analysis of the patterns of spatial and social interaction in combination with genetic relatedness data of wild Guinea baboons (Papio papio), we show that this species exhibits a multilevel social organization in which males maintain strong bonds and are highly tolerant of each other. Several "units" of males with their associated females form "parties," which team up as "gangs." Several gangs of the same "community" use the same home range. Males formed strong bonds predominantly within parties; however, these bonds were not correlated with genetic relatedness. Agonistic interactions were relatively rare and were restricted to a few dyads. Although the social organization of Guinea baboons resembles that of hamadryas baboons, we found stronger male-male affiliation and more elaborate greeting rituals among male Guinea baboons and less aggression toward females. Thus, the social relationships of male Guinea baboons differ markedly from those of other members of the genus, adding valuable comparative data to test hypotheses regarding social evolution. We suggest that this species constitutes an intriguing model to study the predictors and fitness benefits of male bonds, thus contributing to a better understanding of the evolution of this important facet of human social behavior.}, Doi = {10.1073/pnas.1405811111}, Key = {fds227758} } @article{fds321803, Author = {Archie, EA and Tung, J and Clark, M and Altmann, J and Alberts, SC}, Title = {Social affiliation matters: both same-sex and opposite-sex relationships predict survival in wild female baboons.}, Journal = {Proceedings. Biological sciences}, Volume = {281}, Number = {1793}, Pages = {20141261}, Year = {2014}, Month = {October}, url = {http://dx.doi.org/10.1098/rspb.2014.1261}, Abstract = {Social integration and support can have profound effects on human survival. The extent of this phenomenon in non-human animals is largely unknown, but such knowledge is important to understanding the evolution of both lifespan and sociality. Here, we report evidence that levels of affiliative social behaviour (i.e. 'social connectedness') with both same-sex and opposite-sex conspecifics predict adult survival in wild female baboons. In the Amboseli ecosystem in Kenya, adult female baboons that were socially connected to either adult males or adult females lived longer than females who were socially isolated from both sexes--females with strong connectedness to individuals of both sexes lived the longest. Female social connectedness to males was predicted by high dominance rank, indicating that males are a limited resource for females, and females compete for access to male social partners. To date, only a handful of animal studies have found that social relationships may affect survival. This study extends those findings by examining relationships to both sexes in by far the largest dataset yet examined for any animal. Our results support the idea that social effects on survival are evolutionarily conserved in social mammals.}, Doi = {10.1098/rspb.2014.1261}, Key = {fds321803} } @article{fds227756, Author = {Chiyo, PI and Wilson, JW and Archie, EA and Lee, PC and Moss, CJ and Alberts, SC}, Title = {The influence of forage, protected areas, and mating prospects on grouping patterns of male elephants}, Journal = {Behavioral Ecology}, Volume = {25}, Number = {6}, Pages = {1494-1504}, Publisher = {Oxford University Press (OUP)}, Year = {2014}, Month = {September}, ISSN = {1045-2249}, url = {http://dx.doi.org/10.1093/beheco/aru152}, Abstract = {Factors affecting social group size in mammals are relatively well studied for females, but less is known about determinants of group size for males, particularly in species that live in sexually segregated groups. Male grouping patterns are thought to be driven more by spatial and temporal dispersion of mating opportunities than by food resources or predation risk. We evaluated the influence of 3 factors on male group sizes and number of males in mixed-sex groups in African elephants; forage availability (using Normalized Difference Vegetation Index, a satellite-based indicator of primary productivity), anthropogenic mortality risk (using distance of elephants from a protected area center), and mating opportunities (using the number of males in mixed-sex groups with and without estrous females). Using zero-truncated negative binomial regressions and a model-selection approach, we found that male elephants occurred in larger groups where primary productivity was higher and where they were further from a protected area center. However, we found an interaction between primary productivity and anthropogenic mortality risk: at low primary productivity, elephants formed larger groups further away from a protected area center, but did less so at higher primary productivity. This pattern suggests that male elephants are sensitive to seasonal variation in potential anthropogenic mortality risk, by remaining in smaller groups when risk is low, but forming larger groups when risk is high. Mating opportunities also led to an increase in male numbers in mixed-sex groups, but its relative influence on male grouping was less important because mating opportunities were rare.}, Doi = {10.1093/beheco/aru152}, Key = {fds227756} } @article{fds227759, Author = {Lea, AJ and Learn, NH and Theus, MJ and Altmann, J and Alberts, SC}, Title = {Complex sources of variance in female dominance rank in a nepotistic society.}, Journal = {Animal behaviour}, Volume = {94}, Pages = {87-99}, Year = {2014}, Month = {August}, ISSN = {0003-3472}, url = {http://dx.doi.org/10.1016/j.anbehav.2014.05.019}, Abstract = {Many mammalian societies are structured by dominance hierarchies, and an individual's position within this hierarchy can influence reproduction, behaviour, physiology and health. In nepotistic hierarchies, which are common in cercopithecine primates and also seen in spotted hyaenas, <i>Crocuta crocuta</i>, adult daughters are expected to rank immediately below their mother, and in reverse age order (a phenomenon known as 'youngest ascendancy'). This pattern is well described, but few studies have systematically examined the frequency or causes of departures from the expected pattern. Using a longitudinal data set from a natural population of yellow baboons, <i>Papio cynocephalus</i>, we measured the influence of maternal kin, paternal kin and group size on female rank positions at two life history milestones, menarche and first live birth. At menarche, most females (73%) ranked adjacent to their family members (i.e. the female held an ordinal rank in consecutive order with other members of her maternal family); however, only 33% of females showed youngest ascendancy within their matriline at menarche. By the time they experienced their first live birth, many females had improved their dominance rank: 78% ranked adjacent to their family members and 49% showed youngest ascendancy within their matriline. The presence of mothers and maternal sisters exerted a powerful influence on rank outcomes. However, the presence of fathers, brothers and paternal siblings did not produce a clear effect on female dominance rank in our analyses, perhaps because females in our data set co-resided with variable numbers and types of paternal and male relatives. Our results also raise the possibility that female body size or competitive ability may influence dominance rank, even in this classically nepotistic species. In total, our analyses reveal that the predictors of dominance rank in nepotistic rank systems are much more complex than previously thought.}, Doi = {10.1016/j.anbehav.2014.05.019}, Key = {fds227759} } @article{fds227762, Author = {Gesquiere, LR and Ziegler, TE and Chen, PA and Epstein, KA and Alberts, SC and Altmann, J}, Title = {Measuring fecal testosterone in females and fecal estrogens in males: comparison of RIA and LC/MS/MS methods for wild baboons (Papio cynocephalus).}, Journal = {General and comparative endocrinology}, Volume = {204}, Pages = {141-149}, Year = {2014}, Month = {August}, ISSN = {0016-6480}, url = {http://dx.doi.org/10.1016/j.ygcen.2014.04.021}, Abstract = {The development of non-invasive methods, particularly fecal determination, has made possible the assessment of hormone concentrations in wild animal populations. However, measuring fecal metabolites needs careful validation for each species and for each sex. We investigated whether radioimmunoassays (RIAs) previously used to measure fecal testosterone (fT) in male baboons and fecal estrogens (fE) in female baboons were well suited to measure these hormones in the opposite sex. We compared fE and fT concentrations determined by RIA to those measured by liquid chromatography combined with triple quadropole mass spectrometry (LC/MS/MS), a highly specific method. Additionally, we conducted a biological validation to assure that the measurements of fecal concentrations reflected physiological levels of the hormone of interest. Several tests produced expected results that led us to conclude that our RIAs can reliably measure fT and fE in both sexes, and that within-sex comparisons of these measures are valid: (i) fTRIA were significantly correlated to fTLC/MS/MS for both sexes; (ii) fTRIA were higher in adult than in immature males; (iii) fTRIA were higher in pregnant than non-pregnant females; (iv) fERIA were correlated with 17β-estradiol (fE2) and with estrone (fE1) determined by LC/MS/MS in pregnant females; (v) fERIA were significantly correlated with fE2 in non-pregnant females and nearly significantly correlated in males; (vi) fERIA were higher in adult males than in immature males. fERIA were higher in females than in males, as predicted, but unexpectedly, fTRIA were higher in females than in males, suggesting a difference in steroid metabolism in the two sexes; consequently, we conclude that while within-sex comparisons are valid, fTRIA should not be used for intersexual comparisons. Our results should open the field to important additional studies, as to date the roles of testosterone in females and estrogens in males have been little investigated.}, Doi = {10.1016/j.ygcen.2014.04.021}, Key = {fds227762} } @article{fds227760, Author = {Archie, EA and Altmann, J and Alberts, SC}, Title = {Costs of reproduction in a long-lived female primate: injury risk and wound healing.}, Journal = {Behavioral ecology and sociobiology}, Volume = {68}, Number = {7}, Pages = {1183-1193}, Year = {2014}, Month = {July}, ISSN = {0340-5443}, url = {http://dx.doi.org/10.1007/s00265-014-1729-4}, Abstract = {Reproduction is a notoriously costly phase of life, exposing individuals to injury, infectious disease, and energetic tradeoffs. The strength of these costs should be influenced by life history strategies, and in long-lived species, females may be selected to mitigate costs of reproduction because life span is such an important component of their reproductive success. Here we report evidence for two costs of reproduction that may influence survival in wild female baboons-injury risk and delayed wound healing. Based on 29 years of observations in the Amboseli ecosystem, Kenya, we found that wild female baboons experienced the highest risk of injury on days when they were most likely to be ovulating. In addition, lactating females healed from wounds more slowly than pregnant or cycling females, indicating a possible tradeoff between lactation and immune function. We also found variation in injury risk and wound healing with dominance rank and age: older and low-status females were more likely to be injured than younger or high-status females, and older females exhibited slower healing than younger females. Our results support the idea that wild non-human primates experience energetic and immune costs of reproduction, and they help illuminate life history tradeoffs in long-lived species.}, Doi = {10.1007/s00265-014-1729-4}, Key = {fds227760} } @article{fds227761, Author = {Fitzpatrick, CL and Altmann, J and Alberts, SC}, Title = {Sources of variance in a female fertility signal: exaggerated estrous swellings in a natural population of baboons.}, Journal = {Behavioral ecology and sociobiology}, Volume = {68}, Number = {7}, Pages = {1109-1122}, Year = {2014}, Month = {July}, ISSN = {0340-5443}, url = {http://dx.doi.org/10.1007/s00265-014-1722-y}, Abstract = {Signals of fertility in female animals are of increasing interest to evolutionary biologists, a development that coincides with increasing interest in male mate choice and the potential for female traits to evolve under sexual selection. We characterized variation in size of an exaggerated female fertility signal in baboons and investigated the sources of that variance. The number of sexual cycles that a female had experienced after her most recent pregnancy ("cycles since resumption") was the strongest predictor of swelling size. Furthermore, the relationship between cycles since resumption and swelling size was most evident during rainy periods and was not evident during times of drought. Finally, we found significant differences in swelling size between individual females; these differences endured across cycles (i.e., were not explained by variation within individuals) and persisted in spite of ecological effects. This study is the first to provide conclusive evidence of significant variation in swelling size between female primates (controlling for cycles since resumption) and to demonstrate that ecological constraints influence variation in this signal of fertility.}, Doi = {10.1007/s00265-014-1722-y}, Key = {fds227761} } @article{fds227765, Author = {Alberts, SC and Silk, JB}, Title = {The contributions of Jeanne Altmann.}, Journal = {Evolutionary anthropology}, Volume = {22}, Number = {5}, Pages = {198-199}, Year = {2013}, Month = {September}, url = {http://www.ncbi.nlm.nih.gov/pubmed/24166919}, Doi = {10.1002/evan.21370}, Key = {fds227765} } @article{fds227767, Author = {Alberts, SC and Altmann, J and Brockman, DK and Cords, M and Fedigan, LM and Pusey, A and Stoinski, TS and Strier, KB and Morris, WF and Bronikowski, AM}, Title = {Reproductive aging patterns in primates reveal that humans are distinct.}, Journal = {Proceedings of the National Academy of Sciences of the United States of America}, Volume = {110}, Number = {33}, Pages = {13440-13445}, Year = {2013}, Month = {August}, url = {http://www.ncbi.nlm.nih.gov/pubmed/23898189}, Abstract = {Women rarely give birth after ∼45 y of age, and they experience the cessation of reproductive cycles, menopause, at ∼50 y of age after a fertility decline lasting almost two decades. Such reproductive senescence in mid-lifespan is an evolutionary puzzle of enduring interest because it should be inherently disadvantageous. Furthermore, comparative data on reproductive senescence from other primates, or indeed other mammals, remains relatively rare. Here we carried out a unique detailed comparative study of reproductive senescence in seven species of nonhuman primates in natural populations, using long-term, individual-based data, and compared them to a population of humans experiencing natural fertility and mortality. In four of seven primate species we found that reproductive senescence occurred before death only in a small minority of individuals. In three primate species we found evidence of reproductive senescence that accelerated throughout adulthood; however, its initial rate was much lower than mortality, so that relatively few individuals experienced reproductive senescence before death. In contrast, the human population showed the predicted and well-known pattern in which reproductive senescence occurred before death for many women and its rate accelerated throughout adulthood. These results provide strong support for the hypothesis that reproductive senescence in midlife, although apparent in natural-fertility, natural-mortality populations of humans, is generally absent in other primates living in such populations.}, Doi = {10.1073/pnas.1311857110}, Key = {fds227767} } @article{fds227769, Author = {Runcie, DE and Wiedmann, RT and Archie, EA and Altmann, J and Wray, GA and Alberts, SC and Tung, J}, Title = {Social environment influences the relationship between genotype and gene expression in wild baboons.}, Journal = {Philosophical transactions of the Royal Society of London. Series B, Biological sciences}, Volume = {368}, Number = {1618}, Pages = {20120345}, Year = {2013}, Month = {May}, url = {http://www.ncbi.nlm.nih.gov/pubmed/23569293}, Abstract = {Variation in the social environment can have profound effects on survival and reproduction in wild social mammals. However, we know little about the degree to which these effects are influenced by genetic differences among individuals, and conversely, the degree to which social environmental variation mediates genetic reaction norms. To better understand these relationships, we investigated the potential for dominance rank, social connectedness and group size to modify the effects of genetic variation on gene expression in the wild baboons of the Amboseli basin. We found evidence for a number of gene-environment interactions (GEIs) associated with variation in the social environment, encompassing social environments experienced in adulthood as well as persistent effects of early life social environment. Social connectedness, maternal dominance rank and group size all interacted with genotype to influence gene expression in at least one sex, and either in early life or in adulthood. These results suggest that social and behavioural variation, akin to other factors such as age and sex, can impact the genotype-phenotype relationship. We conclude that GEIs mediated by the social environment are important in the evolution and maintenance of individual differences in wild social mammals, including individual differences in responses to social stressors.}, Doi = {10.1098/rstb.2012.0345}, Key = {fds227769} } @article{fds227795, Author = {Onyango, PO and Gesquiere, LR and Altmann, J and Alberts, SC}, Title = {Testosterone positively associated with both male mating effort and paternal behavior in Savanna baboons (Papio cynocephalus).}, Journal = {Hormones and behavior}, Volume = {63}, Number = {3}, Pages = {430-436}, Year = {2013}, Month = {March}, url = {http://www.ncbi.nlm.nih.gov/pubmed/23206991}, Abstract = {Testosterone (T) is often positively associated with male sexual behavior and negatively associated with paternal care. These associations have primarily been demonstrated in species where investment in paternal care begins well after mating activity is complete, when offspring are hatched or born. Different patterns may emerge in studies of species where investment in mating and paternal care overlap temporally, for instance in non-seasonal breeders in which males mate with multiple females sequentially and may simultaneously have multiple offspring of different ages. In a 9-year data set on levels of T in male baboons, fecal concentrations of T (fT) were positively associated with both mate guarding ("consortship") - a measure of current reproductive activity - and with the number of immature offspring a male had in his social group - a measure of past reproductive activity and an indicator of likely paternal behavior. To further examine the relationship between T and potential paternal behavior, we next drew on an intensive 8-month study of male behavior, and found that fathers were more likely to be in close proximity to their offspring than expected by chance. Because male baboons are known to provide paternal care, and because time in proximity to offspring would facilitate such care, this suggests that T concentrations in wild male baboons may be associated with both current reproductive activity and with current paternal behavior. These results are consistent with the predicted positive association between T and mating effort but not with a negative association between T and paternal care; in male baboons, high levels of T occur in males that are differentially associating with their offspring.}, Doi = {10.1016/j.yhbeh.2012.11.014}, Key = {fds227795} } @article{fds227791, Author = {Snyder-Mackler, N and Alberts, SC and Bergman, TJ}, Title = {Concessions of an alpha male? Cooperative defence and shared reproduction in multi-male primate groups.}, Journal = {Proceedings. Biological sciences}, Volume = {279}, Number = {1743}, Pages = {3788-3795}, Year = {2012}, Month = {September}, url = {http://www.ncbi.nlm.nih.gov/pubmed/22764162}, Abstract = {By living in social groups with potential competitors, animals forgo monopolizing access to resources. Consequently, debate continues over how selection might favour sociality among competitors. For example, several models exist to account for the evolution of shared reproduction in groups. The 'concession model' hypothesizes that dominant reproducers benefit from the presence of subordinates, and hence tolerate some reproduction by subordinates. This mutual benefit to both dominants and subordinates may provide a foundation for the formation of social groups in which multiple members reproduce--a necessary step in the evolution of cooperation. To date, however, the concession model has received virtually no support in vertebrates. Instead, the vast majority of vertebrate data support 'limited control models', which posit that dominant reproducers are simply unable to prevent subordinates from reproducing. Here we present the most comprehensive evidence to date in support of the concession model in a vertebrate. We examined natural variation in the number of adult males in gelada (Theropithecus gelada) reproductive units to assess the extent of reproductive skew in multi-male units. Dominant ('leader') males in units that also had subordinate ('follower') males had a 30 per cent longer tenure than leaders in units that did not have followers, mainly because followers actively defended the group against potential immigrants. Follower males also obtained a small amount of reproduction in the unit, which may have functioned as a concession in return for defending the unit. These results suggest that dominants and subordinates may engage in mutually beneficial reproductive transactions, thus favouring male-male tolerance and cooperation.}, Doi = {10.1098/rspb.2012.0842}, Key = {fds227791} } @article{fds227793, Author = {Markham, AC and Alberts, SC and Altmann, J}, Title = {Intergroup conflict: Ecological predictors of winning and consequences of defeat in a wild primate population.}, Journal = {Animal behaviour}, Volume = {82}, Number = {2}, Pages = {399-403}, Publisher = {Elsevier BV}, Year = {2012}, Month = {August}, ISSN = {0003-3472}, url = {http://dx.doi.org/10.1016/j.anbehav.2012.05.009}, Abstract = {In many social species, competition between groups is a major factor proximately affecting group-level movement patterns and space use and ultimately shaping the evolution of group living and complex sociality. Here we evaluated the factors influencing group-level dominance among 5 social groups of wild baboons (Papio cynocephalus), in particular focusing on the spatial determinants of dominance and the consequences of defeat. When direct conflict occurred between conspecific baboon groups, the winning group was predicted by differences in the number of adult males in each group and/or groups that had used the areas surrounding the encounter location more intensively than their opponent in the preceding 9 or 12 months. Relative intensity of space use over shorter timescales examined (3 and 6 months) was a poor predictor of the interaction's outcome. Losing groups but not winning groups experienced clear short-term costs. Losing groups used the area surrounding the interaction less following an agonistic encounter (relative to their intensity of use of the area prior to the interaction). These findings offer insight into the influences and consequences of intergroup competition on group-level patterns of space use.}, Doi = {10.1016/j.anbehav.2012.05.009}, Key = {fds227793} } @article{fds227792, Author = {Tung, J and Charpentier, MJE and Mukherjee, S and Altmann, J and Alberts, SC}, Title = {Genetic effects on mating success and partner choice in a social mammal.}, Journal = {The American naturalist}, Volume = {180}, Number = {1}, Pages = {113-129}, Year = {2012}, Month = {July}, url = {http://www.ncbi.nlm.nih.gov/pubmed/22673655}, Abstract = {Mating behavior has profound consequences for two phenomena--individual reproductive success and the maintenance of species boundaries--that contribute to evolutionary processes. Studies of mating behavior in relation to individual reproductive success are common in many species, but studies of mating behavior in relation to genetic variation and species boundaries are less commonly conducted in socially complex species. Here we leveraged extensive observations of a wild yellow baboon (Papio cynocephalus) population that has experienced recent gene flow from a close sister taxon, the anubis baboon (Papio anubis), to examine how admixture-related genetic background affects mating behavior. We identified novel effects of genetic background on mating patterns, including an advantage accruing to anubis-like males and assortative mating among both yellow-like and anubis-like pairs. These genetic effects acted alongside social dominance rank, inbreeding avoidance, and age to produce highly nonrandom mating patterns. Our results suggest that this population may be undergoing admixture-related evolutionary change, driven in part by nonrandom mating. However, the strength of the genetic effect is mediated by behavioral plasticity and social interactions, emphasizing the strong influence of social context on mating behavior in socially complex species.}, Doi = {10.1086/665993}, Key = {fds227792} } @article{fds227801, Author = {Alberts, SC and Fitzpatrick, CL}, Title = {Paternal care and the evolution of exaggerated sexual swellings in primates.}, Journal = {Behavioral ecology : official journal of the International Society for Behavioral Ecology}, Volume = {23}, Number = {4}, Pages = {699-706}, Year = {2012}, Month = {July}, ISSN = {1045-2249}, url = {http://dx.doi.org/10.1093/beheco/ars052}, Abstract = {The exaggerated sexual swellings exhibited by females of some primate species have been of interest to evolutionary biologists since the time of Darwin. We summarize existing hypotheses for their function and evolution and categorize these hypotheses within the context of 3 types of variation in sexual swelling size: 1) variation within a single sexual cycle, 2) variation between the sexual cycles of a single female, and 3) differences between females. We then propose the Paternal Care Hypothesis for the function of sexual swellings, which posits that exaggerated sexual swellings function to elicit the right quantity and quality of male care for a female's infant. As others have noted, swellings may allow females to engender paternity confusion, or they may allow females to confer relative paternal certainty on one male. Key to our hypothesis is that both of these scenarios create an incentive for one or more males to provide care. This hypothesis builds on previous hypotheses but differs from them by highlighting the elicitation of paternal care as a key function of swellings. Our hypothesis predicts that true paternal care (in which males accurately differentiate and provide assistance to their own offspring) will be most common in species in which exaggerated swellings accurately signal the probability of conception, and males can monopolize females during the window of highest conception probability. Our hypothesis also predicts that females will experience selection to behave in ways that either augment paternity confusion or enhance paternal certainty depending on their social and demographic contexts.}, Doi = {10.1093/beheco/ars052}, Key = {fds227801} } @article{fds227794, Author = {Archie, EA and Altmann, J and Alberts, SC}, Title = {Social status predicts wound healing in wild baboons.}, Journal = {Proceedings of the National Academy of Sciences of the United States of America}, Volume = {109}, Number = {23}, Pages = {9017-9022}, Year = {2012}, Month = {June}, ISSN = {0027-8424}, url = {http://dx.doi.org/10.1073/pnas.1206391109}, Abstract = {Social status can have striking effects on health in humans and other animals, but the causes often are unknown. In male vertebrates, status-related differences in health may be influenced by correlates of male social status that suppress immune responses. Immunosuppressive correlates of low social status may include chronic social stress, poor physical condition, and old age; the immunosuppressive correlates of high status may include high testosterone and energetic costs of reproduction. Here we test whether these correlates could create status-related differences in immune function by measuring the incidence of illness and injury and then examining healing rates in a 27-y data set of natural injuries and illnesses in wild baboon males. We found no evidence that the high testosterone and intense reproductive effort associated with high rank suppress immune responses. Instead, high-ranking males were less likely to become ill, and they recovered more quickly than low-ranking males, even controlling for differences in age. Notably, alpha males, who experience high glucocorticoids, as well as the highest testosterone and reproductive effort, healed significantly faster than other males, even other high-ranking males. We discuss why alpha males seem to escape from the immunosuppressive costs of glucocorticoids but low-ranking males do not, including the idea that glucocorticoids' effects depend on an individual's physiological and social context.}, Doi = {10.1073/pnas.1206391109}, Key = {fds227794} } @article{fds227802, Author = {Silk, JB and Alberts, SC and Altmann, J and Cheney, DL and Seyfarth, RM}, Title = {Stability of partner choice among female baboons.}, Journal = {Animal behaviour}, Volume = {83}, Number = {6}, Pages = {1511-1518}, Year = {2012}, Month = {June}, ISSN = {0003-3472}, url = {http://dx.doi.org/10.1016/j.anbehav.2012.03.028}, Abstract = {In a wide range of taxa, including baboons, close social bonds seem to help animals cope with stress and enhance long-term reproductive success and longevity. Current evidence suggests that female baboons may benefit from establishing and maintaining highly individuated relationships with a relatively small number of partners. Here, we extend previous work on the stability of female baboons' social relationships in three different ways. First, we assess the stability of females' social relationships in two distinct and geographically distant sites using the same method. Second, we conduct simulations to determine whether females' social relationships were more stable than expected by chance. Third, we examine demographic sources of variance in the stability of close social bonds. At both sites, females' relationships with their most preferred partners were significantly more stable than expected by chance. In contrast, their relationships with less preferred partners were more ephemeral, often changing from year to year. While nearly all females experienced some change in their top partners across time, many maintained relationships with top partners for several years. Females that lived in smaller groups and had more close kin available had more stable social relationships than those that lived in larger groups and had fewer close kin available.}, Doi = {10.1016/j.anbehav.2012.03.028}, Key = {fds227802} } @article{fds227800, Author = {Nguyen, N and Gesquiere, L and Alberts, SC and Altmann, J}, Title = {Sex differences in the mother-neonate relationship in wild baboons: Social, experiential and hormonal correlates}, Journal = {Animal Behaviour}, Volume = {83}, Number = {4}, Pages = {891-903}, Publisher = {Elsevier BV}, Year = {2012}, Month = {April}, ISSN = {0003-3472}, url = {http://dx.doi.org/10.1016/j.anbehav.2012.01.003}, Abstract = {In mammals, maternal care is essential for offspring survival, yet individual differences in this care can dramatically affect offspring growth and development. Few studies have, however, investigated the sources, magnitude and consequences of naturally occurring interindividual variation in maternal care during the neonatal period. In this study, we examine several hormonal and nonhormonal predictors of naturally occurring variation in the mother-neonate relationship during the first 8. weeks of infancy in 34 wild baboon (. Papio cynocephalus) mother-infant dyads in Amboseli, Kenya. We use data on physical contact and suckling patterns to assess the quality of the mother-neonate relationship and to evaluate the extent to which variation in this relationship is predictable from perinatal ovarian steroids (i.e. faecal oestrogen and progesterone metabolites), previous infant care experience, maternal dominance rank and offspring sex. We found that newborn infants of more experienced mothers initiated higher rates of changes in mother-infant contact than newborns of less experienced mothers. However, at each level of maternal experience, newborn males initiated higher rates of changes in mother-infant contact than newborn females. Moreover, we found evidence suggesting that variation in suckling activity among daughters (but not sons) was predictable from maternal dominance rank and faecal oestrogen (fE) concentrations before birth. To our knowledge, our study provides the first evidence of (1) the influence of cumulative maternal experience on the mother-infant relationship and (2) the emergence of sex differences in the mother-infant relationship during the neonatal period in wild primates. Our results suggest that the well-documented sex differences in life history, behaviour and ecology in primates (and other social mammals) may originate very early in life. © 2012 The Association for the Study of Animal Behaviour.}, Doi = {10.1016/j.anbehav.2012.01.003}, Key = {fds227800} } @article{fds227797, Author = {Charpentier, MJE and Fontaine, MC and Cherel, E and Renoult, JP and Jenkins, T and Benoit, L and Barthès, N and Alberts, SC and Tung, J}, Title = {Genetic structure in a dynamic baboon hybrid zone corroborates behavioural observations in a hybrid population.}, Journal = {Molecular ecology}, Volume = {21}, Number = {3}, Pages = {715-731}, Year = {2012}, Month = {February}, ISSN = {0962-1083}, url = {http://dx.doi.org/10.1111/j.1365-294x.2011.05302.x}, Abstract = {Behaviour and genetic structure are intimately related: mating patterns and patterns of movement between groups or populations influence the movement of genetic variation across the landscape and from one generation to the next. In hybrid zones, the behaviour of the hybridizing taxa can also impact the incidence and outcome of hybridization events. Hybridization between yellow baboons and anubis baboons has been well documented in the Amboseli basin of Kenya, where more anubis-like individuals tend to experience maturational and reproductive advantages. However, it is unknown whether these advantages are reflected in the genetic structure of populations surrounding this area. Here, we used microsatellite genotype data to evaluate the structure and composition of baboon populations in southern Kenya. Our results indicate that, unlike for mitochondrial DNA, microsatellite-based measures of genetic structure concord with phenotypically based taxonomic distinctions and that the currently active hybrid zone is relatively narrow. Isolation with migration analysis revealed asymmetric gene flow in this region from anubis populations into yellow populations, in support of the anubis-biased phenotypic advantages observed in Amboseli. Populations that are primarily yellow but that receive anubis gene flow exhibit higher levels of genetic diversity than yellow populations far from the introgression front. Our results support previous work that indicates a long history of hybridization and introgression among East African baboons. Specifically, it suggests that anubis baboons are in the process of gradual range expansion into the range of yellow baboons, a pattern potentially explained by behavioural and life history advantages that correlate with anubis ancestry.}, Doi = {10.1111/j.1365-294x.2011.05302.x}, Key = {fds227797} } @article{fds227790, Author = {Harper, KN and Fyumagwa, RD and Hoare, R and Wambura, PN and Coppenhaver, DH and Sapolsky, RM and Alberts, SC and Tung, J and Rogers, J and Kilewo, M and Batamuzi, EK and Leendertz, FH and Armelagos, GJ and Knauf, S}, Title = {Treponema pallidum infection in the wild baboons of East Africa: distribution and genetic characterization of the strains responsible.}, Journal = {PloS one}, Volume = {7}, Number = {12}, Pages = {e50882}, Year = {2012}, Month = {January}, ISSN = {1932-6203}, url = {http://gateway.webofknowledge.com/gateway/Gateway.cgi?GWVersion=2&SrcApp=PARTNER_APP&SrcAuth=LinksAMR&KeyUT=WOS:000312794500017&DestLinkType=FullRecord&DestApp=ALL_WOS&UsrCustomerID=47d3190e77e5a3a53558812f597b0b92}, Abstract = {It has been known for decades that wild baboons are naturally infected with Treponema pallidum, the bacterium that causes the diseases syphilis (subsp. pallidum), yaws (subsp. pertenue), and bejel (subsp. endemicum) in humans. Recently, a form of T. pallidum infection associated with severe genital lesions has been described in wild baboons at Lake Manyara National Park in Tanzania. In this study, we investigated ten additional sites in Tanzania and Kenya using a combination of macroscopic observation and serology, in order to determine whether the infection was present in each area. In addition, we obtained genetic sequence data from six polymorphic regions using T. pallidum strains collected from baboons at two different Tanzanian sites. We report that lesions consistent with T. pallidum infection were present at four of the five Tanzanian sites examined, and serology was used to confirm treponemal infection at three of these. By contrast, no signs of treponemal infection were observed at the six Kenyan sites, and serology indicated T. pallidum was present at only one of them. A survey of sexually mature baboons at Lake Manyara National Park in 2006 carried out as part of this study indicated that roughly ten percent displayed T. pallidum-associated lesions severe enough to cause major structural damage to the genitalia. Finally, we found that T. pallidum strains from Lake Manyara National Park and Serengeti National Park were genetically distinct, and a phylogeny suggested that baboon strains may have diverged prior to the clade containing human strains. We conclude that T. pallidum infection associated with genital lesions appears to be common in the wild baboons of the regions studied in Tanzania. Further study is needed to elucidate the infection's transmission mode, its associated morbidity and mortality, and the relationship between baboon and human strains.}, Doi = {10.1371/journal.pone.0050882}, Key = {fds227790} } @article{fds227798, Author = {Chiyo, PI and Moss, CJ and Alberts, SC}, Title = {The influence of life history milestones and association networks on crop-raiding behavior in male African elephants.}, Journal = {PloS one}, Volume = {7}, Number = {2}, Pages = {e31382}, Year = {2012}, Month = {January}, url = {http://www.ncbi.nlm.nih.gov/pubmed/22347468}, Abstract = {Factors that influence learning and the spread of behavior in wild animal populations are important for understanding species responses to changing environments and for species conservation. In populations of wildlife species that come into conflict with humans by raiding cultivated crops, simple models of exposure of individual animals to crops do not entirely explain the prevalence of crop raiding behavior. We investigated the influence of life history milestones using age and association patterns on the probability of being a crop raider among wild free ranging male African elephants; we focused on males because female elephants are not known to raid crops in our study population. We examined several features of an elephant association network; network density, community structure and association based on age similarity since they are known to influence the spread of behaviors in a population. We found that older males were more likely to be raiders than younger males, that males were more likely to be raiders when their closest associates were also raiders, and that males were more likely to be raiders when their second closest associates were raiders older than them. The male association network had sparse associations, a tendency for individuals similar in age and raiding status to associate, and a strong community structure. However, raiders were randomly distributed between communities. These features of the elephant association network may limit the spread of raiding behavior and likely determine the prevalence of raiding behavior in elephant populations. Our results suggest that social learning has a major influence on the acquisition of raiding behavior in younger males whereas life history factors are important drivers of raiding behavior in older males. Further, both life-history and network patterns may influence the acquisition and spread of complex behaviors in animal populations and provide insight on managing human-wildlife conflict.}, Doi = {10.1371/journal.pone.0031382}, Key = {fds227798} } @article{fds227799, Author = {Babbitt, CC and Tung, J and Wray, GA and Alberts, SC}, Title = {Changes in gene expression associated with reproductive maturation in wild female baboons.}, Journal = {Genome biology and evolution}, Volume = {4}, Number = {2}, Pages = {102-109}, Year = {2012}, Month = {January}, ISSN = {1759-6653}, url = {http://dx.doi.org/10.1093/gbe/evr134}, Abstract = {Changes in gene expression during development play an important role in shaping morphological and behavioral differences, including between humans and nonhuman primates. Although many of the most striking developmental changes occur during early development, reproductive maturation represents another critical window in primate life history. However, this process is difficult to study at the molecular level in natural primate populations. Here, we took advantage of ovarian samples made available through an unusual episode of human-wildlife conflict to identify genes that are important in this process. Specifically, we used RNA sequencing (RNA-Seq) to compare genome-wide gene expression patterns in the ovarian tissue of juvenile and adult female baboons from Amboseli National Park, Kenya. We combined this information with prior evidence of selection occurring on two primate lineages (human and chimpanzee). We found that in cases in which genes were both differentially expressed over the course of ovarian maturation and also linked to lineage-specific selection this selective signature was much more likely to occur in regulatory regions than in coding regions. These results suggest that adaptive change in the development of the primate ovary may be largely driven at the mechanistic level by selection on gene regulation, potentially in relationship to the physiology or timing of female reproductive maturation.}, Doi = {10.1093/gbe/evr134}, Key = {fds227799} } @article{fds227763, Author = {Rodrigo, A and Alberts, S and Cranston, K and Kingsolver, J and Lapp, H and McClain, C and Smith, R and Vision, T and Weintraub, J and Wiegmann, B}, Title = {Science incubators: synthesis centers and their role in the research ecosystem}, Journal = {PLoS Biology}, Volume = {11}, Number = {1}, Pages = {e1001468}, Year = {2012}, url = {http://hdl.handle.net/10161/10193 Duke open access}, Abstract = {How should funding agencies enable researchers to explore high-risk but potentially high-reward science? One model that appears to work is the NSF-funded synthesis center, an incubator for community-led, innovative science.}, Doi = {10.1371/journal.pbio.1001468}, Key = {fds227763} } @article{fds227796, Author = {Akinyi, MY and Tung, J and Jenneby, M and Patel, NB and Altmann, J and Alberts, SC}, Title = {Role of grooming in reducing tick load in wild baboons (Papio cynocephalus)}, Journal = {Animal Behaviour}, Volume = {85}, Number = {3}, Pages = {559-568}, Year = {2012}, url = {http://dx.doi.org/10.1016/j.anbehav.2012.12.012}, Abstract = {Nonhuman primate species spend a conspicuous amount of time grooming during social interactions, a behavior that probably serves both social and health-related functions. While the social implications of grooming have been relatively well studied, less attention has been paid to the health benefits, especially the removal of ectoparasites, which may act as vectors in disease transmission. In this study, we examined the relationship between grooming behavior, tick load (number of ticks), and haemoprotozoan infection status in a population of wild free-ranging baboons (<i>Papio cynocephalus</i>). We found that the amount of grooming received was influenced by an individual's age, sex and dominance rank. The amount of grooming received, in turn, affected the tick load of an individual. Baboons with higher tick loads had lower packed red cell volume (PCV or haematocrit), one general measure of health status. We detected a tick-borne haemoprotozoan, <i>Babesia microti</i>, but its low prevalence in the population precluded identifying sources of variance in infection.}, Doi = {10.1016/j.anbehav.2012.12.012}, Key = {fds227796} } @article{fds227803, Author = {Markham, AC and Alberts, SC and Altmann, J}, Title = {When good neighbors don't need fences: Temporal landscape partitioning among baboon social groups}, Journal = {Behavioral Ecology and Sociobiology}, Volume = {67}, Number = {6}, Pages = {875-884}, Year = {2012}, ISSN = {0340-5443}, url = {http://dx.doi.org/10.1007/s00265-013-1510-0}, Abstract = {Intraspecific competition is a key factor shaping space-use strategies and movement decisions in many species, yet how and when neighbors utilize shared areas while exhibiting active avoidance of one another is largely unknown. Here we investigated temporal landscape partitioning in a population of wild baboons (<i>Papio cynocephalus</i>). We used global positioning system (GPS) collars to synchronously record the hourly locations of 5 baboon social groups for ~900 days, and we used behavioral, demographic, and life history data to measure factors affecting use of overlap areas. Annual home ranges of neighboring groups overlapped substantially, as predicted (baboons are considered non-territorial), but home ranges overlapped less when space use was assessed over shorter time scales. Moreover, neighboring groups were in close spatial proximity to one another on fewer days than predicted by a null model, suggesting an avoidance-based spacing pattern. At all time scales examined (monthly, biweekly, and weekly), time spent in overlap areas was greater during time periods when groups fed on evenly dispersed, low-quality foods. The percent of fertile females in social groups was negatively correlated with time spent in overlap areas only during weekly time intervals. This suggests that broad temporal changes in ecological resources are a major predictor of how intensively overlap areas are used, and groups modify these ecologically driven spacing patterns at short time scales based on female reproductive status. Together these findings offer insight into the economics of territoriality by highlighting the dynamics of spacing patterns at differing time scales.}, Doi = {10.1007/s00265-013-1510-0}, Key = {fds227803} } @article{fds227804, Author = {Onyango, PO and Alberts, SC and Altmann, J}, Title = {Season and female reproductive quality but not opportunities for paternal care predict intensity of male mate guarding in a non-seasonally breeding primate. Behavioral Ecology and Sociobiology.}, Journal = {Behavioral Ecology and Sociobiology}, Year = {2012}, Key = {fds227804} } @article{fds227805, Author = {Onyango, PO and Gesquiere, L and Altmann, J and Alberts, SC}, Title = {Puberty and dispersal in a wild primate population}, Journal = {Hormones and Behavior}, Volume = {64}, Number = {2}, Pages = {240-249}, Year = {2012}, url = {http://dx.doi.org/10.1016/j.yhbeh.2013.02.014}, Abstract = {This article is part of a Special Issue "Puberty and Adolescence". The onset of reproduction is preceded by a host of organismal adjustments and transformations, involving morphological, physiological, and behavioral changes. In highly social mammals, including humans and most nonhuman primates, the timing and nature of maturational processes are affected by the animal's social milieu as well as its ecology. Here, we review a diverse set of findings on how maturation unfolds in wild baboons in the Amboseli basin of southern Kenya, and we place these findings in the context of other reports of maturational processes in primates and other mammals. First, we describe the series of events and processes that signal maturation in female and male baboons. Sex differences in age at both sexual maturity and first reproduction documented for this species are consistent with expectations of life history theory; males mature later than females and exhibit an adolescent growth spurt that is absent or minimal in females. Second, we summarize what we know about sources of variance in the timing of maturational processes including natal dispersal. In Amboseli, individuals in a food-enhanced group mature earlier than their wild-feeding counterparts, and offspring of high-ranking females mature earlier than offspring of low-ranking females. We also report on how genetic admixture, which occurs in Amboseli between two closely related baboon taxa, affects individual maturation schedules.}, Doi = {10.1016/j.yhbeh.2013.02.014}, Key = {fds227805} } @article{fds304249, Author = {Markham, AC and Gesquiere, LR and Bellenger, J-P and Alberts, SC and Altmann, J}, Title = {White monkey syndrome and presumptive copper deficiency in wild savannah baboons.}, Journal = {American journal of primatology}, Volume = {73}, Number = {11}, Pages = {1160-1168}, Year = {2011}, Month = {November}, ISSN = {0275-2565}, url = {http://dx.doi.org/10.1002/ajp.20983}, Abstract = {In immature wild savannah baboons (Papio cynocephalus), we observed symptoms consistent with copper (Cu) deficiency and, more specifically, with a disorder referred to as white monkey syndrome (WMS) in laboratory primates. The objectives of this study were to characterize this pathology, and test three hypotheses that (1) Cu deficiency may have been induced by zinc (Zn) toxicity, (2) it may have been induced by molybdenum (Mo) toxicity, and (3) cumulative rainfall during the perinatal period and particularly during gestation is an ecological factor distinguishing infants afflicted with WMS from non-WMS infants. During 2001-2009, we observed 22 instances of WMS out of a total 377 live births in the study population. Visible symptoms exhibited by WMS infants included whitening of the animal's fur and/or impaired mobility characterized by an apparent "stiffening" of the hindlimbs. Occurrence of WMS did not vary significantly by gender. However, among individuals that survived at least 180 days, WMS males had a significantly lower survivorship probability than non-WMS males. Zn/Cu ratios assessed from hair samples of adult female baboons were higher in females who had produced at least one WMS offspring relative to females who had not had a WMS offspring. This was true even when the hair sample was collected long after the birth of the female's afflicted infant. We consider this potentially indicative of a robust tendency for low Cu levels induced by elevated Zn intake in some individuals. No significant differences of Mo/Cu ratios were observed. Cumulative rainfall during gestation (∼179 days) was 50% lower for WMS infants relative to non-WMS infants. In contrast, rainfall for the two classes of infants did not differ in the 180 days before conception or in the 180 days following birth. This finding highlights the importance of prenatal ecological conditions in healthy fetal development with regard to WMS.}, Doi = {10.1002/ajp.20983}, Key = {fds304249} } @article{fds304247, Author = {Gesquiere, LR and Learn, NH and Simao, MCM and Onyango, PO and Alberts, SC and Altmann, J}, Title = {Life at the top: rank and stress in wild male baboons.}, Journal = {Science (New York, N.Y.)}, Volume = {333}, Number = {6040}, Pages = {357-360}, Year = {2011}, Month = {July}, ISSN = {0036-8075}, url = {http://dx.doi.org/10.1126/science.1207120}, Abstract = {In social hierarchies, dominant individuals experience reproductive and health benefits, but the costs of social dominance remain a topic of debate. Prevailing hypotheses predict that higher-ranking males experience higher testosterone and glucocorticoid (stress hormone) levels than lower-ranking males when hierarchies are unstable but not otherwise. In this long-term study of rank-related stress in a natural population of savannah baboons (Papio cynocephalus), high-ranking males had higher testosterone and lower glucocorticoid levels than other males, regardless of hierarchy stability. The singular exception was for the highest-ranking (alpha) males, who exhibited both high testosterone and high glucocorticoid levels. In particular, alpha males exhibited much higher stress hormone levels than second-ranking (beta) males, suggesting that being at the very top may be more costly than previously thought.}, Doi = {10.1126/science.1207120}, Key = {fds304247} } @article{fds227808, Author = {Chiyo, PI and Moss, CJ and Archie, EA and Hollister-Smith, JA and Alberts, SC}, Title = {Using molecular and observational techniques to estimate the number and raiding patterns of crop-raiding elephants}, Journal = {Journal of Applied Ecology}, Volume = {48}, Number = {3}, Pages = {788-796}, Publisher = {WILEY}, Year = {2011}, Month = {June}, ISSN = {0021-8901}, url = {http://dx.doi.org/10.1111/j.1365-2664.2011.01967.x}, Abstract = {1. Conflict between humans and animals, generated by behaviours like crop raiding, can represent a major threat to the survival and conservation of protected species. Crop raiding is an example where the conflict is assumed to be attributable to a small number of habitually raiding animals. No studies have systematically tested this assumption on African elephants Loxodonta africana. 2. In the greater Amboseli basin, in southern Kenya, we determined the number of elephants that come into conflict with humans through crop raiding, their gender, and their patterns of raiding. We tracked footprints, and observed elephants after they raided farms, and genotyped DNA extracted from faeces collected from raided farms. Using these data, we estimated the number of raiders with asymptotic regression and count models. 3. We found that 241 elephants from several elephant populations in the Amboseli basin raided farms. Raiders were independent males; we detected no females raiding crops. Approximately 35% of the raiders were from the Amboseli elephant population, representing about 1/3 of the independent males in that population. Approximately 12% of raiders from the Amboseli elephant population were habitual and were responsible for 56% of elephant raiding events. 4. Synthesis and applications. Our results suggest that targeted elimination of habitual raiders could in theory reduce crop raiding. However, the large pool of occasional raiders, the availability of palatable crops in areas of conflict, and the link between crop-raiding and natural male foraging tactics, indicates great potential for recruitment of habitual raiders from this pool of occasional raiders. Furthermore, shooting of raiders as a strategy for reducing crop raiding carries a high risk of misidentifying habitual raiders. We suggest instead an ethical management strategy that uses remote monitoring of raiders as an early warning system for crop protection, and longitudinal studies to evaluate the development of habitual raiding. © 2011 The Authors. Journal of Applied Ecology © 2011 British Ecological Society.}, Doi = {10.1111/j.1365-2664.2011.01967.x}, Key = {fds227808} } @article{fds304248, Author = {Chiyo, PI and Archie, EA and Hollister-Smith, JA and Lee, PC and Poole, JH and Moss, CJ and Alberts, SC}, Title = {Association patterns of African elephants in all-male groups: The role of age and genetic relatedness}, Journal = {Animal Behaviour}, Volume = {81}, Number = {6}, Pages = {1093-1099}, Publisher = {Elsevier BV}, Year = {2011}, Month = {June}, ISSN = {0003-3472}, url = {http://dx.doi.org/10.1016/j.anbehav.2011.02.013}, Abstract = {Strong social bonds are uncommon among male mammals. In many mammals, however, males form all-male groups, providing opportunities for male-male bonds to emerge. We examined association patterns of male African elephants, Loxodonta africana, in all-male groups and assessed the influence of age and genetic relatedness on these associations. We also examined the influence of age and genetic relatedness on the choice of sparring partners in male elephants. Males had many weak and random associations and few valuable relationships. Male associations were positively correlated with genetic relatedness, suggesting that kinship influences patterns of male associations. Male associations were negatively correlated with age disparity, and males were more likely to spar with other males closer in age to themselves. These results suggest that males associate with other males of similar age in part because sparring may facilitate the development and maintenance of motor and psychological responses to sudden and unexpected events that occur during play; this may help prepare males for male-male competition. We also found that older males had high centrality and strength in social networks, suggesting that older males influence the cohesion of male social groups. Consequently, the elimination of older males from elephant populations by poachers or trophy hunters could negatively affect social cohesion in male elephant groups. Finally, we found that age and genetic relatedness were not significantly correlated, suggesting that male associations based on age and relatedness did not overlap. These findings highlight the complexity of male social relationships in all-male groups. © 2011 The Association for the Study of Animal Behaviour.}, Doi = {10.1016/j.anbehav.2011.02.013}, Key = {fds304248} } @article{fds227810, Author = {Bronikowski, AM and Altmann, J and Brockman, DK and Cords, M and Fedigan, LM and Pusey, A and Stoinski, T and Morris, WF and Strier, KB and Alberts, SC}, Title = {Aging in the natural world: comparative data reveal similar mortality patterns across primates.}, Journal = {Science (New York, N.Y.)}, Volume = {331}, Number = {6022}, Pages = {1325-1328}, Year = {2011}, Month = {March}, ISSN = {0036-8075}, url = {http://dx.doi.org/10.1126/science.1201571}, Abstract = {Human senescence patterns-late onset of mortality increase, slow mortality acceleration, and exceptional longevity-are often described as unique in the animal world. Using an individual-based data set from longitudinal studies of wild populations of seven primate species, we show that contrary to assumptions of human uniqueness, human senescence falls within the primate continuum of aging; the tendency for males to have shorter life spans and higher age-specific mortality than females throughout much of adulthood is a common feature in many, but not all, primates; and the aging profiles of primate species do not reflect phylogenetic position. These findings suggest that mortality patterns in primates are shaped by local selective forces rather than phylogenetic history.}, Doi = {10.1126/science.1201571}, Key = {fds227810} } @article{fds227807, Author = {Tung, J and Akinyi, MY and Mutura, S and Altmann, J and Wray, GA and Alberts, SC}, Title = {Allele-specific gene expression in a wild nonhuman primate population.}, Journal = {Molecular ecology}, Volume = {20}, Number = {4}, Pages = {725-739}, Year = {2011}, Month = {February}, url = {http://www.ncbi.nlm.nih.gov/pubmed/21226779}, Abstract = {Natural populations hold enormous potential for evolutionary genetic studies, especially when phenotypic, genetic and environmental data are all available on the same individuals. However, untangling the genotype-phenotype relationship in natural populations remains a major challenge. Here, we describe results of an investigation of one class of phenotype, allele-specific gene expression (ASGE), in the well-studied natural population of baboons of the Amboseli basin, Kenya. ASGE measurements identify cases in which one allele of a gene is overexpressed relative to the alternative allele of the same gene, within individuals, thus providing a control for background genetic and environmental effects. Here, we characterize the incidence of ASGE in the Amboseli baboon population, focusing on the genetic and environmental contributions to ASGE in a set of eleven genes involved in immunity and defence. Within this set, we identify evidence for common ASGE in four genes. We also present examples of two relationships between cis-regulatory genetic variants and the ASGE phenotype. Finally, we identify one case in which this relationship is influenced by a novel gene-environment interaction. Specifically, the dominance rank of an individual's mother during its early life (an aspect of that individual's social environment) influences the expression of the gene CCL5 via an interaction with cis-regulatory genetic variation. These results illustrate how environmental and ecological data can be integrated into evolutionary genetic studies of functional variation in natural populations. They also highlight the potential importance of early life environmental variation in shaping the genetic architecture of complex traits in wild mammals.}, Doi = {10.1111/j.1365-294x.2010.04970.x}, Key = {fds227807} } @article{fds227815, Author = {Gesquiere, LR and Onyango, PO and Alberts, SC and Altmann, J}, Title = {Endocrinology of year-round reproduction in a highly seasonal habitat: environmental variability in testosterone and glucocorticoids in baboon males.}, Journal = {American journal of physical anthropology}, Volume = {144}, Number = {2}, Pages = {169-176}, Year = {2011}, Month = {February}, ISSN = {0002-9483}, url = {http://dx.doi.org/10.1002/ajpa.21374}, Abstract = {In conditions characterized by energetic constraints, such as in periods of low food availability, some trade-offs between reproduction and self-maintenance may be necessary; even year-round breeders may then be forced to exhibit some reproductive seasonality. Prior research has largely focused on female reproduction and physiology, and few studies have evaluated the impact of environmental factors on males. Here we assessed the effects of season and ambient temperatures on fecal glucocorticoid (fGC) and testosterone (fT) levels in male baboons in Amboseli, Kenya. The Amboseli basin is a highly challenging, semiarid tropical habitat that is characterized by strongly seasonal patterns of rainfall and by high ambient temperatures. We previously reported that female baboons were impacted by these challenging environmental conditions. We ask here whether male baboons in the same environment and groups as females exhibit similar physiological effects. We found that after accounting for male age and individual variability, males exhibited higher fGC levels and lower fT levels during the dry season than during the wet season. Furthermore, fT but not fGC levels were lower in months of high average daily maximum temperatures, suggesting a direct impact of heat on testes. Our results demonstrate that male baboons, like females, experience ecological stress that alters their reproductive physiology. The impact of the environment on male reproduction deserves more attention both in its own right and because alteration in male physiology may contribute to the reduction in female fertility observed inchallenging environments.}, Doi = {10.1002/ajpa.21374}, Key = {fds227815} } @article{fds227814, Author = {Morris, WF and Altmann, J and Brockman, DK and Cords, M and Fedigan, LM and Pusey, AE and Stoinski, TS and Bronikowski, AM and Alberts, SC and Strier, KB}, Title = {Low demographic variability in wild primate populations: fitness impacts of variation, covariation, and serial correlation in vital rates.}, Journal = {The American naturalist}, Volume = {177}, Number = {1}, Pages = {E14-E28}, Year = {2011}, Month = {January}, url = {http://www.ncbi.nlm.nih.gov/pubmed/21117962}, Abstract = {In a stochastic environment, long-term fitness can be influenced by variation, covariation, and serial correlation in vital rates (survival and fertility). Yet no study of an animal population has parsed the contributions of these three aspects of variability to long-term fitness. We do so using a unique database that includes complete life-history information for wild-living individuals of seven primate species that have been the subjects of long-term (22-45 years) behavioral studies. Overall, the estimated levels of vital rate variation had only minor effects on long-term fitness, and the effects of vital rate covariation and serial correlation were even weaker. To explore why, we compared estimated variances of adult survival in primates with values for other vertebrates in the literature and found that adult survival is significantly less variable in primates than it is in the other vertebrates. Finally, we tested the prediction that adult survival, because it more strongly influences fitness in a constant environment, will be less variable than newborn survival, and we found only mixed support for the prediction. Our results suggest that wild primates may be buffered against detrimental fitness effects of environmental stochasticity by their highly developed cognitive abilities, social networks, and broad, flexible diets.}, Doi = {10.1086/657443}, Key = {fds227814} } @article{fds227816, Author = {Galbany, J and Altmann, J and Perez Perez and A and Alberts, SC}, Title = {Age and individual foraging behavior predict tooth wear in Amboseli baboons}, Journal = {American Journal of Physical Anthropology}, Volume = {144}, Number = {1}, Pages = {51-59}, Year = {2011}, Month = {January}, url = {http://www.ncbi.nlm.nih.gov/pubmed/20721946}, Abstract = {Teeth represent an essential component of the foraging apparatus for any mammal, and tooth wear can have significant implications for survival and reproduction. This study focuses on tooth wear in wild baboons in Amboseli, southern Kenya. We obtained mandibular and maxillary tooth impressions from 95 baboons and analyzed digital images of replicas made from these impressions. We measured tooth wear as the percent dentine exposure (PDE, the percent of the occlusal surface on which dentine was exposed), and we examined the relationship of PDE to age, behavior, and life history variables. We found that PDE increased significantly with age for both sexes in all three molar types. In females, we also tested the hypotheses that long-term patterns of feeding behavior, social dominance rank, and one measure of maternal investment (the cumulative number of months that a female had dependent infants during her lifetime) would predict tooth wear when we controlled for age. The hypothesis that feeding behavior predicted tooth wear was supported. The percent of feeding time spent consuming grass corms predicted PDE when controlling for age. However, PDE was not associated with social dominance rank or maternal investment.}, Doi = {10.1002/ajpa.21368}, Key = {fds227816} } @article{fds227806, Author = {Markham, AC and Gesquiere, LR and Bellenger, JP and Alberts, SC and Altmann, J}, Title = {White Monkey Syndrome and presumptive copper deficiency in a wild primate population}, Journal = {American Journal of Primatology}, Volume = {73}, Number = {11}, Pages = {1-9}, Year = {2011}, ISSN = {0275-2565}, url = {http://dx.doi.org/10.1002/ajp.20983}, Abstract = {In immature wild savannah baboons (Papio cynocephalus), we observed symptoms consistent with copper (Cu) deficiency and, more specifically, with a disorder referred to as white monkey syndrome (WMS) in laboratory primates. The objectives of this study were to characterize this pathology, and test three hypotheses that (1) Cu deficiency may have been induced by zinc (Zn) toxicity, (2) it may have been induced by molybdenum (Mo) toxicity, and (3) cumulative rainfall during the perinatal period and particularly during gestation is an ecological factor distinguishing infants afflicted with WMS from non-WMS infants. During 2001-2009, we observed 22 instances of WMS out of a total 377 live births in the study population. Visible symptoms exhibited by WMS infants included whitening of the animal's fur and/or impaired mobility characterized by an apparent "stiffening" of the hindlimbs. Occurrence of WMS did not vary significantly by gender. However, among individuals that survived at least 180 days, WMS males had a significantly lower survivorship probability than non-WMS males. Zn/Cu ratios assessed from hair samples of adult female baboons were higher in females who had produced at least one WMS offspring relative to females who had not had a WMS offspring. This was true even when the hair sample was collected long after the birth of the female's afflicted infant. We consider this potentially indicative of a robust tendency for low Cu levels induced by elevated Zn intake in some individuals. No significant differences of Mo/Cu ratios were observed. Cumulative rainfall during gestation (~179 days) was 50% lower for WMS infants relative to non-WMS infants. In contrast, rainfall for the two classes of infants did not differ in the 180 days before conception or in the 180 days following birth. This finding highlights the importance of prenatal ecological conditions in healthy fetal development with regard to WMS. © 2011 Wiley Periodicals, Inc.}, Doi = {10.1002/ajp.20983}, Key = {fds227806} } @article{fds227809, Author = {Galbany, J and Dotras, L and Altmann, J and Alberts, SC and Perez Perez, A}, Title = {Tooth size variation related to age in Amboseli baboons}, Journal = {Folia Primatologica}, Volume = {81}, Number = {6}, Pages = {348-359}, Year = {2011}, url = {http://www.ncbi.nlm.nih.gov/pubmed/21325862}, Abstract = {We measured the molar size from a single population of wild baboons from Amboseli (Kenya), both females (n=57) and males (n=50). All the females were of known age; the males represented a mix of known-age individuals (n=31) and individuals with ages estimated to within 2 years (n=19). The results showed a significant reduction in the mesiodistal length of teeth in both sexes as a function of age. Overall patterns of age-related change in tooth size did not change whether we included or excluded the individuals of estimated age, but patterns of statistical significance changed as a result of changed sample sizes. Our results demonstrate that tooth length is directly related to age due to interproximal wearing caused by M2 and M3 compression loads. Dental studies in primates, including both fossil and extant species, are mostly based on specimens obtained from osteological collections of varying origins, for which the age at death of each individual in the sample is not known. Researchers should take into account the phenomenon of interproximal attrition leading to reduced tooth size when measuring tooth length for ondontometric purposes.}, Doi = {10.1159/000323588}, Key = {fds227809} } @article{fds227811, Author = {Gesquiere, LR and Learn, NH and Simao, MCM and Onyango, PO and Alberts, SC and Altmann, J}, Title = {Life at the top: energetic and psychological stress in wild male primates}, Journal = {Science}, Volume = {333}, Number = {6040}, Pages = {357-360}, Year = {2011}, ISSN = {0036-8075}, url = {http://dx.doi.org/10.1126/science.1207120}, Abstract = {In social hierarchies, dominant individuals experience reproductive and health benefits, but the costs of social dominance remain a topic of debate. Prevailing hypotheses predict that higher-ranking males experience higher testosterone and glucocorticoid (stress hormone) levels than lower-ranking males when hierarchies are unstable but not otherwise. In this long-term study of rank-related stress in a natural population of savannah baboons (Papio cynocephalus), high-ranking males had higher testosterone and lower glucocorticoid levels than other males, regardless of hierarchy stability. The singular exception was for the highest-ranking (alpha) males, who exhibited both high testosterone and high glucocorticoid levels. In particular, alpha males exhibited much higher stress hormone levels than second-ranking (beta) males, suggesting that being at the very top may be more costly than previously thought.}, Doi = {10.1126/science.1207120}, Key = {fds227811} } @article{fds227812, Author = {Chiyo, PI and Archie, EA and Hollister Smith and JA and Lee, PC and Poole, JH and Moss, CJ and Alberts, SC}, Title = {Association patterns of male African elephants: the role of age and genetic relatedness}, Journal = {Animal Behaviour}, Volume = {81}, Number = {6}, Pages = {1093-1099}, Year = {2011}, ISSN = {0003-3472}, url = {http://dx.doi.org/10.1016/j.anbehav.2011.02.013}, Abstract = {Strong social bonds are uncommon among male mammals. In many mammals, however, males form all-male groups, providing opportunities for male-male bonds to emerge. We examined association patterns of male African elephants, Loxodonta africana, in all-male groups and assessed the influence of age and genetic relatedness on these associations. We also examined the influence of age and genetic relatedness on the choice of sparring partners in male elephants. Males had many weak and random associations and few valuable relationships. Male associations were positively correlated with genetic relatedness, suggesting that kinship influences patterns of male associations. Male associations were negatively correlated with age disparity, and males were more likely to spar with other males closer in age to themselves. These results suggest that males associate with other males of similar age in part because sparring may facilitate the development and maintenance of motor and psychological responses to sudden and unexpected events that occur during play; this may help prepare males for male-male competition. We also found that older males had high centrality and strength in social networks, suggesting that older males influence the cohesion of male social groups. Consequently, the elimination of older males from elephant populations by poachers or trophy hunters could negatively affect social cohesion in male elephant groups. Finally, we found that age and genetic relatedness were not significantly correlated, suggesting that male associations based on age and relatedness did not overlap. These findings highlight the complexity of male social relationships in all-male groups. © 2011 The Association for the Study of Animal Behaviour.}, Doi = {10.1016/j.anbehav.2011.02.013}, Key = {fds227812} } @article{fds227813, Author = {Chiyo, PI and Lee, PC and Moss, CJ and Archie, EA and Hollister Smith, JA and Alberts, SC}, Title = {No risk, no gain: effects of crop-raiding and genetic heterozygosity on body size in male African elephants}, Journal = {Behavioral Ecology and Sociobiology}, Volume = {22}, Number = {3}, Pages = {552-558}, Publisher = {Oxford University Press (OUP)}, Year = {2011}, ISSN = {1045-2249}, url = {http://dx.doi.org/10.1093/beheco/arr016}, Abstract = {Body size is an important influence on the life history of males of polygynous mammals because it is usually highly correlated with fitness and is under intense selection. In this paper, we investigated the effect of high-risk foraging behavior (crop raiding) and genetic heterozygosity on male body size in a well-studied population of African elephants. Crop raiding, the foraging on cultivated food crops by wildlife is one of the main causes of wildlife human conflict and is a major conservation issue for many polygynous mammals that live in proximity to agriculture or human habitation. Body size was estimated using hind foot size, a measure strongly correlated with stature and mass. Crop raiding predicted male size in adulthood, with raiders being larger than nonraiders. However, elephants that became raiders were neither larger nor smaller for age when young. Enhanced growth rates and size among raiders suggest that taking risks pays off for males. Lastly, genetic heterozygosity had no effect on size for age in male elephants, most likely because low-heterozygosity males were rare. Risky foraging behavior can evolve as a result of strong sexual selection for large size and condition-dependent mating success in males. We discuss the implications of these results for managing human-wildlife conflict. © The Author 2011.}, Doi = {10.1093/beheco/arr016}, Key = {fds227813} } @article{fds227785, Author = {Alberts, SC}, Title = {Primatology: "a faithful friend is the medicine of life".}, Journal = {Current biology : CB}, Volume = {20}, Number = {15}, Pages = {R632-R634}, Year = {2010}, Month = {August}, url = {http://www.ncbi.nlm.nih.gov/pubmed/20692609}, Abstract = {Close, stable social bonds enhance longevity in wild baboons, providing clues about the importance of social bonds in our own evolutionary history.}, Doi = {10.1016/j.cub.2010.06.012}, Key = {fds227785} } @article{fds227818, Author = {Tung, J and Alberts, SC and Wray, GA}, Title = {Evolutionary genetics in wild primates: combining genetic approaches with field studies of natural populations.}, Journal = {Trends in genetics : TIG}, Volume = {26}, Number = {8}, Pages = {353-362}, Year = {2010}, Month = {August}, ISSN = {0168-9525}, url = {http://www.ncbi.nlm.nih.gov/pubmed/20580115}, Abstract = {Ecological and evolutionary studies of wild primates hold important keys to understanding both the shared characteristics of primate biology and the genetic and phenotypic differences that make specific lineages, including our own, unique. Although complementary genetic research on nonhuman primates has long been of interest, recent technological and methodological advances now enable functional and population genetic studies in an unprecedented manner. In the past several years, novel genetic data sets have revealed new information about the demographic history of primate populations and the genetics of adaptively important traits. In combination with the rich history of behavioral, ecological, and physiological work on natural primate populations, genetic approaches promise to provide a compelling picture of primate evolution in the past and in the present day.}, Doi = {10.1016/j.tig.2010.05.005}, Key = {fds227818} } @article{fds227821, Author = {Altmann, J and Gesquiere, L and Galbany, J and Onyango, PO and Alberts, SC}, Title = {Life history context of reproductive aging in a wild primate model.}, Journal = {Annals of the New York Academy of Sciences}, Volume = {1204}, Pages = {127-138}, Year = {2010}, Month = {August}, ISSN = {0077-8923}, url = {http://dx.doi.org/10.1111/j.1749-6632.2010.05531.x}, Abstract = {The pace of reproductive aging has been of considerable interest, especially in regard to the long postreproductive period in modern women. Here we use data for both sexes from a 37-year longitudinal study of a wild baboon population to place reproductive aging within a life history context for this species, a primate relative of humans that evolved in the same savannah habitat as humans did. We examine the patterns and pace of reproductive aging, including birth rates and reproductive hormones for both sexes, and compare reproductive aging to age-related changes in several other traits. Reproductive senescence occurs later in baboon females than males. Delayed senescence in females relative to males is also found in several other traits, such as dominance status and body condition, but not in molar wear or glucocorticoid profiles. Survival, health, and well-being are the product of risk factors in morphological, physiological, and behavioral traits that differ in rate of senescence and in dependence on social or ecological conditions; some will be very sensitive to differences in circumstances and others less so.}, Doi = {10.1111/j.1749-6632.2010.05531.x}, Key = {fds227821} } @article{fds227819, Author = {Strier, KB and Altmann, J and Brockman, DK and Bronikowski, AM and Cords, M and Fedigan, LM and Lapp, H and Liu, X and Morris, WF and Pusey, AE and Stoinski, TS and Alberts, SC}, Title = {The Primate Life History Database: A unique shared ecological data resource.}, Journal = {Methods in ecology and evolution}, Volume = {1}, Number = {2}, Pages = {199-211}, Year = {2010}, Month = {June}, ISSN = {2041-210X}, url = {http://gateway.webofknowledge.com/gateway/Gateway.cgi?GWVersion=2&SrcApp=PARTNER_APP&SrcAuth=LinksAMR&KeyUT=WOS:000288914100013&DestLinkType=FullRecord&DestApp=ALL_WOS&UsrCustomerID=47d3190e77e5a3a53558812f597b0b92}, Abstract = {The importance of data archiving, data sharing, and public access to data has received considerable attention. Awareness is growing among scientists that collaborative databases can facilitate these activities.We provide a detailed description of the collaborative life history database developed by our Working Group at the National Evolutionary Synthesis Center (NESCent) to address questions about life history patterns and the evolution of mortality and demographic variability in wild primates.Examples from each of the seven primate species included in our database illustrate the range of data incorporated and the challenges, decision-making processes, and criteria applied to standardize data across diverse field studies. In addition to the descriptive and structural metadata associated with our database, we also describe the process metadata (how the database was designed and delivered) and the technical specifications of the database.Our database provides a useful model for other researchers interested in developing similar types of databases for other organisms, while our process metadata may be helpful to other groups of researchers interested in developing databases for other types of collaborative analyses.}, Doi = {10.1111/j.2041-210x.2010.00023.x}, Key = {fds227819} } @article{fds304246, Author = {Wasser, S and Poole, J and Lee, P and Lindsay, K and Dobson, A and Hart, J and Douglas-Hamilton, I and Wittemyer, G and Granli, P and Morgan, B and Gunn, J and Alberts, S and Beyers, R and Chiyo, P and Croze, H and Estes, R and Gobush, K and Joram, P and Kikoti, A and Kingdon, J and King, L and Macdonald, D and Moss, C and Mutayoba, B and Njumbi, S and Omondi, P and Nowak, K}, Title = {Conservation. Elephants, ivory, and trade.}, Journal = {Science (New York, N.Y.)}, Volume = {327}, Number = {5971}, Pages = {1331-1332}, Year = {2010}, Month = {March}, ISSN = {0036-8075}, url = {http://dx.doi.org/10.1126/science.1187811}, Abstract = {Trade decisions made by the Convention on International Trade in Endangered Species must place science over politics.}, Doi = {10.1126/science.1187811}, Key = {fds304246} } @article{fds227820, Author = {Archie, EA and Henry, T and Maldonado, JE and Moss, CJ and Poole, JH and Pearson, VR and Murray, S and Alberts, SC and Fleischer, RC}, Title = {Major histocompatibility complex variation and evolution at a single, expressed DQA locus in two genera of elephants.}, Journal = {Immunogenetics}, Volume = {62}, Number = {2}, Pages = {85-100}, Year = {2010}, Month = {February}, ISSN = {0093-7711}, url = {http://dx.doi.org/10.1007/s00251-009-0413-8}, Abstract = {Genes of the vertebrate major histocompatibility complex (MHC) are crucial to defense against infectious disease, provide an important measure of functional genetic diversity, and have been implicated in mate choice and kin recognition. As a result, MHC loci have been characterized for a number of vertebrate species, especially mammals;however, elephants are a notable exception. Our study is the first to characterize patterns of genetic diversity and natural selection in the elephant MHC. We did so using DNA sequences from a single, expressed DQA locus in elephants.We characterized six alleles in 30 African elephants(Loxodonta africana) and four alleles in three Asian elephants (Elephas maximus). In addition, for two of the African alleles and three of the Asian alleles, we characterized complete coding sequences (exons 1-5) and nearly complete non-coding sequences (introns 2-4) for the class II DQA loci. Compared to DQA in other wild mammals, we found moderate polymorphism and allelic diversity and similar patterns of selection; patterns of non-synonymous and synonymous substitutions were consistent with balancing selection acting on the peptides involved in antigen binding in the second exon. In addition, balancing selection has led to strong trans-species allelism that has maintained multiple allelic lineages across both genera of extant elephants for at least 6 million years. We discuss our results in the context of MHC diversity in other mammals and patterns of evolution in elephants.}, Doi = {10.1007/s00251-009-0413-8}, Key = {fds227820} } @article{fds227817, Author = {Wasser, S and Poole, J and Lee, P and Kindsay, K and Dobson, A and Hart, J and Douglas Hamilton and I and Wittemyer, G and Granli, P and Morgan, B and Gunn, J and Alberts, S and Beyers, R and Chiyo, P and Croze, H and Estes, R and Gobush, K and Joram, P and Kikoti, A and Kingdon, J and King, L and Macdonald, D and Moss, C and Mutayoba, B and Numbi, S and Omondi, P and Nowak, K}, Title = {Policy Forum: Elephants, Ivory and Trade}, Journal = {Science}, Volume = {327}, Number = {5971}, Pages = {1331-1332}, Year = {2010}, ISSN = {0036-8075}, url = {http://dx.doi.org/10.1126/science.1187811}, Abstract = {Trade decisions made by the Convention on International Trade in Endangered Species must place science over politics.}, Doi = {10.1126/science.1187811}, Key = {fds227817} } @article{fds227783, Author = {Chiyo, PI and Alberts, SC}, Title = {An assessment of the threat to Grevy's zebra from hybridization}, Journal = {Animal Conservation}, Volume = {12}, Number = {6}, Pages = {514-515}, Publisher = {WILEY}, Year = {2009}, Month = {December}, ISSN = {1367-9430}, url = {http://dx.doi.org/10.1111/j.1469-1795.2009.00333.x}, Doi = {10.1111/j.1469-1795.2009.00333.x}, Key = {fds227783} } @article{fds227823, Author = {Beehner, JC and Gesquiere, L and Seyfarth, RM and Cheney, DL and Alberts, SC and Altmann, J}, Title = {Testosterone related to age and life-history stages in male baboons and geladas.}, Journal = {Hormones and behavior}, Volume = {56}, Number = {4}, Pages = {472-480}, Year = {2009}, Month = {October}, ISSN = {0018-506X}, url = {http://dx.doi.org/10.1016/j.yhbeh.2009.08.005}, Abstract = {Despite significant advances in our knowledge of how testosterone mediates life-history trade-offs, this research has primarily focused on seasonal taxa. We know comparatively little about the relationship between testosterone and life-history stages for non-seasonally breeding species. Here we examine testosterone profiles across the life span of males from three non-seasonally breeding primates: yellow baboons (Papio cynocephalus or P. hamadryas cynocephalus), chacma baboons (Papio ursinus or P. h. ursinus), and geladas (Theropithecus gelada). First, we predict that testosterone profiles will track the reproductive profiles of each taxon across their respective breeding years. Second, we evaluate age-related changes in testosterone to determine whether several life-history transitions are associated with these changes. Subjects include males (>2.5 years) from wild populations of each taxon from whom we had fecal samples for hormone determination. Although testosterone profiles across taxa were broadly similar, considerable variability was found in the timing of two major changes: (1) the attainment of adult levels of testosterone and (2) the decline in testosterone after the period of maximum production. Attainment of adult testosterone levels was delayed by 1 year in chacmas compared with yellows and geladas. With respect to the decline in testosterone, geladas and chacmas exhibited a significant drop after 3 years of maximum production, while yellows declined so gradually that no significant annual drop was ever detected. For both yellows and chacmas, increases in testosterone production preceded elevations in social dominance rank. We discuss these differences in the context of ecological and behavioral differences exhibited by these taxa.}, Doi = {10.1016/j.yhbeh.2009.08.005}, Key = {fds227823} } @article{fds227822, Author = {Nguyen, N and Van Horn and RC and Alberts, SC and Altmann, J}, Title = {"Friendships" between new mothers and adult males: adaptive benefits and determinants in wild baboons (Papio cynocephalus).}, Journal = {Behavioral ecology and sociobiology}, Volume = {63}, Number = {9}, Pages = {1331-1344}, Year = {2009}, Month = {July}, ISSN = {0340-5443}, url = {http://dx.doi.org/10.1007/s00265-009-0786-6}, Abstract = {Close associations between adult males and lactating females and their dependent infants are not commonly described in non-monogamous mammals. However, such associations [sometimes called "friendships" (Smuts 1985)] are regularly observed in several primate species in which females mate with multiple males during the fertile period. The absence of mating exclusivity among "friends" suggests that males should invest little in infant care, raising questions about the adaptive significance of friendship bonds. Using data from genetic paternity analyses, patterns of behavior, and long-term demographic and reproductive records, we evaluated the extent to which friendships in four multi-male, multi-female yellow baboon (<i>Papio cynocephalus</i>) groups in Amboseli, Kenya represent joint parental care of offspring or male mating effort. We found evidence that mothers and infants benefited directly from friendships; friendships provided mother-infant dyads protection from harassment from other adult and immature females. In addition, nearly half of all male friends were the genetic fathers of offspring and had been observed mating with mothers during the days of most likely conception for those offspring. In contrast, nearly all friends who were not fathers were also not observed to consort with the mother during the days of most likely conception, suggesting that friendships between mothers and non-fathers did not result from paternity confusion. Finally, we found no evidence that prior friendship increased a male's chances of mating with a female in future reproductive cycles. Our results suggest that, for many male-female pairs at Amboseli, friendships represented a form of biparental care of offspring. Males in the remaining friendship dyads may be trading protection of infants in exchange for some resources or services not yet identified. Our study is the first to find evidence that female primates gain social benefits from their early associations with adult males.}, Doi = {10.1007/s00265-009-0786-6}, Key = {fds227822} } @article{fds227824, Author = {Tung, J and Primus, A and Bouley, AJ and Severson, TF and Alberts, SC and Wray, GA}, Title = {Evolution of a malaria resistance gene in wild primates.}, Journal = {Nature}, Volume = {460}, Number = {7253}, Pages = {388-391}, Year = {2009}, Month = {July}, url = {http://www.ncbi.nlm.nih.gov/pubmed/19553936}, Abstract = {The ecology, behaviour and genetics of our closest living relatives, the nonhuman primates, should help us to understand the evolution of our own lineage. Although a large amount of data has been amassed on primate ecology and behaviour, much less is known about the functional and evolutionary genetic aspects of primate biology, especially in wild primates. As a result, even in well-studied populations in which nongenetic factors that influence adaptively important characteristics have been identified, we have almost no understanding of the underlying genetic basis for such traits. Here, we report on the functional consequences of genetic variation at the malaria-related FY (DARC) gene in a well-studied population of yellow baboons (Papio cynocephalus) living in Amboseli National Park in Kenya. FY codes for a chemokine receptor normally expressed on the erythrocyte surface that is the known entry point for the malarial parasite Plasmodium vivax. We identified variation in the cis-regulatory region of the baboon FY gene that was associated with phenotypic variation in susceptibility to Hepatocystis, a malaria-like pathogen that is common in baboons. Genetic variation in this region also influenced gene expression in vivo in wild individuals, a result we confirmed using in vitro reporter gene assays. The patterns of genetic variation in and around this locus were also suggestive of non-neutral evolution, raising the possibility that the evolution of the FY cis-regulatory region in baboons has exhibited both mechanistic and selective parallels with the homologous region in humans. Together, our results represent the first reported association and functional characterization linking genetic variation and a complex trait in a natural population of nonhuman primates.}, Doi = {10.1038/nature08149}, Key = {fds227824} } @article{fds227825, Author = {Hollister Smith and JA and Alberts, SC and Rasmussen, LEL}, Title = {Do male African elephants (Loxodonta africana) signal musth via urine dribbling?}, Journal = {Animal Behaviour}, Volume = {76}, Number = {6}, Pages = {1829-1841}, Publisher = {Elsevier BV}, Year = {2008}, Month = {December}, ISSN = {0003-3472}, url = {http://dx.doi.org/10.1016/j.anbehav.2008.05.033}, Abstract = {The phenomenon of musth in male elephants involves increased sexual activity, heightened aggression and nearly continuous dribbling of pungent smelling urine. Urine chemistry during musth is altered, suggesting that urine may signal the musth status of the individual. Signalling musth remotely may benefit individuals if it reduces the likelihood of physical confrontation between males, which can lead to injury and even death. Few studies, however, have asked whether and how male elephants respond to urine of other males. We tested two predictions of the hypothesis that urine signals musth status to male conspecifics: (1) that male African elephants differentiate musth and nonmusth urine, and (2) that males differentiate between urine dribbled during early and late musth. The second prediction stems from the observation that males lose weight and presumably body condition during musth. We conducted two related bioassays with 26 captive nonmusth males ranging from 13 to 52 years of age. In each assay, subjects were simultaneously presented with three urine samples (nonmusth, early musth, late musth), each from a different donor male, and a control. We found that subjects differentiated between musth and nonmusth samples using their vomeronasal organ system, but did not discriminate between the samples using their main olfactory system. Males did not differentiate early from late musth. In addition, we found that subject contextual factors, specifically age, dominance status and social grouping, significantly predicted response. We discuss these results within the framework of male elephant longevity and social relationships and their importance to reproductive success. © 2008 The Association for the Study of Animal Behaviour.}, Doi = {10.1016/j.anbehav.2008.05.033}, Key = {fds227825} } @article{fds227826, Author = {Onyango, PO and Gesquiere, LR and Wango, EO and Alberts, SC and Altmann, J}, Title = {Persistence of maternal effects in baboons: Mother's dominance rank at son's conception predicts stress hormone levels in subadult males.}, Journal = {Hormones and behavior}, Volume = {54}, Number = {2}, Pages = {319-324}, Year = {2008}, Month = {August}, ISSN = {0018-506X}, url = {http://dx.doi.org/10.1016/j.yhbeh.2008.03.002}, Abstract = {Dominance status and reproductive experience are maternal characteristics that affect offspring traits in diverse taxa, including some cercopithecine primates. Maternal effects of this sort are widespread and are sources of variability in offspring fitness. We tested the hypothesis that maternal dominance rank and reproductive experience as well as a male's own age and dominance rank predicted chronic fecal glucocorticoid (fGC) concentrations in 17 subadult wild male baboons, Papio cynocephalus (median age 6.5 years), in the Amboseli basin, Kenya. Among these variables, maternal dominance rank at a subadult male's conception was the sole significant predictor of the male's fGC and accounted for 42% of fGC variance; sons of lower ranking mothers had higher fGC than did those of high-ranking mothers. This result is striking because subadult male baboons are approximately 4-6 years past the period of infant dependence on their mothers, and are larger than and dominant to all adult females. In addition, many males of this age have survived their mothers' death. Consequently, the influence of maternal dominance rank persisted well beyond the stage at which direct maternal influence on sons is likely. Persistence of these major maternal influences from the perinatal period may signal organizational effects of mothers on sons' HPA axis. Although short-term, acute, elevations in GC are part of adaptive responses to challenges such as predators and other emergencies, chronically elevated GC are often associated with stress-related pathologies and, thereby, adverse effects on fitness components.}, Doi = {10.1016/j.yhbeh.2008.03.002}, Key = {fds227826} } @article{fds304245, Author = {Gesquiere, LR and Khan, M and Shek, L and Wango, TL and Wango, EO and Alberts, SC and Altmann, J}, Title = {Coping with a challenging environment: effects of seasonal variability and reproductive status on glucocorticoid concentrations of female baboons (Papio cynocephalus).}, Journal = {Hormones and behavior}, Volume = {54}, Number = {3}, Pages = {410-416}, Year = {2008}, Month = {August}, ISSN = {0018-506X}, url = {http://dx.doi.org/10.1016/j.yhbeh.2008.04.007}, Abstract = {Environmental stressors impact physiology and behavior in many species of animals. These effects are partly mediated through changing concentrations of glucocorticoids, which also vary with reproductive state and social conditions. Prior research has focused largely on seasonal breeders, but the close temporal linkage between season and reproductive state in these species hinders ability to disentangle environmental effects from those of the animal's reproductive status. Here we assessed the effects of environmental challenges on the fecal glucocorticoid (fGC) levels of non-seasonal breeders, female baboons (Papio cynocephalus) of Amboseli, Kenya. Amboseli is characterized by a long dry season, during which food and water become scarce, and by extreme temperatures above 40 degrees C in the shade during some months of the year. We found that after accounting for female reproductive status and individual variability, females exhibited higher fGC levels during the dry season than during the wet season. Further, during the wet season, fGC levels were higher in months of high average daily maximum temperatures. During the dry season, fGC levels were elevated both in hotter months and in months during which the baboons spent a relatively high proportion of time feeding. In spite of these stressors, female baboons reproduce during all months of the year in Amboseli, unlike most other mammals in this environment. This may be attributable to their extreme adaptability, specifically their diversified diet, and their ability to modify their behavior, including their activity profiles.}, Doi = {10.1016/j.yhbeh.2008.04.007}, Key = {fds304245} } @article{fds227829, Author = {Archie, EA and Maldonado, JE and Hollister-Smith, JA and Poole, JH and Moss, CJ and Fleischer, RC and Alberts, SC}, Title = {Fine-scale population genetic structure in a fission-fusion society.}, Journal = {Molecular ecology}, Volume = {17}, Number = {11}, Pages = {2666-2679}, Year = {2008}, Month = {June}, ISSN = {0962-1083}, url = {http://dx.doi.org/10.1111/j.1365-294x.2008.03797.x}, Abstract = {Nonrandom patterns of mating and dispersal create fine-scale genetic structure in natural populations - especially of social mammals - with important evolutionary and conservation genetic consequences. Such structure is well-characterized for typical mammalian societies; that is, societies where social group composition is stable, dispersal is male-biased, and males form permanent breeding associations in just one or a few social groups over the course of their lives. However, genetic structure is not well understood for social mammals that differ from this pattern, including elephants. In elephant societies, social groups fission and fuse, and males never form permanent breeding associations with female groups. Here, we combine 33 years of behavioural observations with genetic information for 545 African elephants (Loxodonta africana), to investigate how mating and dispersal behaviours structure genetic variation between social groups and across age classes. We found that, like most social mammals, female matrilocality in elephants creates co-ancestry within core social groups and significant genetic differentiation between groups (Phi(ST) = 0.058). However, unlike typical social mammals, male elephants do not bias reproduction towards a limited subset of social groups, and instead breed randomly across the population. As a result, reproductively dominant males mediate gene flow between core groups, which creates cohorts of similar-aged paternal relatives across the population. Because poaching tends to eliminate the oldest elephants from populations, illegal hunting and poaching are likely to erode fine-scale genetic structure. We discuss our results and their evolutionary and conservation genetic implications in the context of other social mammals.}, Doi = {10.1111/j.1365-294x.2008.03797.x}, Key = {fds227829} } @article{fds227828, Author = {Nguyen, N and Gesquiere, LR and Wango, EO and Alberts, SC and Altmann, J}, Title = {Late pregnancy glucocorticoid levels predict responsiveness in wild baboon mothers (Papio cynocephalus)}, Journal = {Animal Behaviour}, Volume = {75}, Number = {5}, Pages = {1747-1756}, Publisher = {Elsevier BV}, Year = {2008}, Month = {May}, ISSN = {0003-3472}, url = {http://dx.doi.org/10.1016/j.anbehav.2007.09.035}, Abstract = {Maternal care is the most significant measure of successful adaptation among female mammals. Understanding the predictors of individual differences in offspring care is a major objective of mammalian reproductive biology. Recent studies suggest that differences in caregiving motivation may be associated with variation in glucocorticoid (GC) hormones in new mothers. Despite these intriguing reports, questions remain about the stability of this association during a period of rapid change in both behaviour and physiology, about whether this relationship is dependent on other nonhormonal variables and about the generality of this pattern across species and in wild populations. Glucocorticoids modulate animals' responses to ongoing stressors and may also prepare animals for predictable future challenges. We evaluated evidence for both actions of GCs on maternal responsiveness towards infant cries during the first 2 months of infancy in 34 wild baboon mother-infant dyads in Amboseli, Kenya. We found that stable individual differences in faecal GCs during late pregnancy predicted stable individual differences in maternal responsiveness after birth, even after controlling for maternal rank and parity, and infant sex and distress rate. This study is among the first to provide evidence of preparative actions of GCs in wild animals and to show stability of behavioural and hormonal traits during a period of rapid changes in both hormones and behaviour. Because elevations in GCs during late pregnancy are probably primarily of fetal rather than maternal origin, our results raise the intriguing possibility that parent-offspring conflict may underlie the preparative actions of GCs on maternal responsiveness to infant distress. © 2008 The Association for the Study of Animal Behaviour.}, Doi = {10.1016/j.anbehav.2007.09.035}, Key = {fds227828} } @article{fds227830, Author = {Charpentier, MJE and Tung, J and Altmann, J and Alberts, SC}, Title = {Age at maturity in wild baboons: genetic, environmental and demographic influences.}, Journal = {Molecular ecology}, Volume = {17}, Number = {8}, Pages = {2026-2040}, Year = {2008}, Month = {April}, url = {http://www.ncbi.nlm.nih.gov/pubmed/18346122}, Abstract = {The timing of early life-history events, such as sexual maturation and first reproduction, can greatly influence variation in individual fitness. In this study, we analysed possible sources of variation underlying different measures of age at social and physical maturation in wild baboons in the Amboseli basin, Kenya. The Amboseli baboons are a natural population primarily comprised of yellow baboons (Papio cynocephalus) that occasionally hybridize with anubis baboons (Papio anubis) from outside the basin. We found that males and females differed in the extent to which various factors influenced their maturation. Surprisingly, we found that male maturation was most strongly related to the proportion of anubis ancestry revealed by their microsatellite genotypes: hybrid males matured earlier than yellow males. In contrast, although hybrid females reached menarche slightly earlier than yellow females, maternal rank and the presence of maternal relatives had the largest effects on female maturation, followed by more modest effects of group size and rainfall. Our results indicate that a complex combination of demographic, genetic, environmental, and maternal effects contribute to variation in the timing of these life-history milestones.}, Doi = {10.1111/j.1365-294x.2008.03724.x}, Key = {fds227830} } @article{fds227831, Author = {Tung, J and Charpentier, MJE and Garfield, DA and Altmann, J and Alberts, SC}, Title = {Genetic evidence reveals temporal change in hybridization patterns in a wild baboon population.}, Journal = {Molecular ecology}, Volume = {17}, Number = {8}, Pages = {1998-2011}, Year = {2008}, Month = {April}, url = {http://www.ncbi.nlm.nih.gov/pubmed/18363664}, Abstract = {The process and consequences of hybridization are of interest to evolutionary biologists because of the importance of hybridization in understanding reproductive isolation, speciation, and the influence of introgression on population genetic structure. Recent studies of hybridization have been enhanced by the advent of sensitive, genetic marker-based techniques for inferring the degree of admixture occurring within individuals. Here we present a genetic marker-based analysis of hybridization in a large-bodied, long-lived mammal over multiple generations. We analysed patterns of hybridization between yellow baboons (Papio cynocephalus) and anubis baboons (Papio anubis) in a well-studied natural population in Amboseli National Park, Kenya, using genetic samples from 450 individuals born over the last 36 years. We assigned genetic hybrid scores based on genotypes at 14 microsatellite loci using the clustering algorithm implemented in STRUCTURE 2.0, and assessed the robustness of these scores by comparison to pedigree information and through simulation. The genetic hybrid scores showed generally good agreement with previous morphological assessments of hybridity, but suggest that genetic methods may be more sensitive for identification of low levels of hybridity. The results of our analysis indicate that the proportion of hybrids in the Amboseli population has grown over time, but that the average proportion of anubis ancestry within hybrids is gradually decreasing. We argue that these patterns are probably a result of both selective and nonselective processes, including differences in the timing of life-history events for hybrid males relative to yellow baboon males, and stochasticity in long-distance dispersal from the source anubis population into Amboseli.}, Doi = {10.1111/j.1365-294x.2008.03723.x}, Key = {fds227831} } @article{fds227832, Author = {Charpentier, MJE and Van Horn and RC and Altmann, J and Alberts, SC}, Title = {Paternal effects on offspring fitness in a multimale primate society.}, Journal = {Proceedings of the National Academy of Sciences of the United States of America}, Volume = {105}, Number = {6}, Pages = {1988-1992}, Year = {2008}, Month = {February}, url = {http://www.ncbi.nlm.nih.gov/pubmed/18250308}, Abstract = {When females mate with multiple males, paternal care is generally expected to be negligible, because it may be difficult or impossible for males to discriminate their own offspring from those of other males, and because engaging in paternal care may reduce male mating opportunities. Consequently, males in multimale societies are not predicted to provide direct benefits to their offspring. We have recently demonstrated, however, that males in a typical multimale primate society (yellow baboons, Papio cynocephalus) discriminate their own offspring from those of other males and provide care to them in the form of repeated support during agonistic encounters. This observation raises the question of whether fathers enhance offspring fitness in this species. Here we use 30 years of data on age at maturity for 118 yellow baboons with known fathers. We show that the father's presence in the offspring's social group during the offspring's immature period accelerated the timing of physiological maturation in daughters. Sons also experienced accelerated maturation if their father was present during their immature period, but only if the father was high ranking at the time of their birth. Because age at reproductive maturity has a large impact on lifetime reproductive success, our results indicate a direct effect of paternal presence on offspring fitness. This relationship in turn suggests that the multiple roles that males play in multimale animal societies have not been sufficiently examined or appreciated and that paternal effects may be more pervasive than previously appreciated.}, Doi = {10.1073/pnas.0711219105}, Key = {fds227832} } @article{fds227833, Author = {Van Horn and RC and Altmann, J and Alberts, SC}, Title = {Can't get there from here: inferring kinship from pairwise genetic relatedness}, Journal = {Animal Behaviour}, Volume = {75}, Number = {3}, Pages = {1173-1180}, Publisher = {Elsevier BV}, Year = {2008}, Month = {January}, ISSN = {0003-3472}, url = {http://dx.doi.org/10.1016/j.anbehav.2007.08.027}, Doi = {10.1016/j.anbehav.2007.08.027}, Key = {fds227833} } @article{fds352880, Author = {Widdig, A and Alberts, SC and Nuernberg, P and Krawzcak, M}, Title = {Do mothers promote social preference among their paternally related offspring? Testing mechanisms of paternal kin discrimination}, Journal = {FOLIA PRIMATOLOGICA}, Volume = {79}, Number = {5}, Pages = {398-398}, Publisher = {KARGER}, Year = {2008}, Month = {January}, Key = {fds352880} } @article{fds227789, Author = {Alberts, S}, Title = {Why play by the rules? Constitutionalism and democratic institutionalization in Ecuador and Uruguay}, Journal = {Democratization}, Volume = {15}, Number = {5}, Pages = {849-869}, Publisher = {Informa UK Limited}, Year = {2008}, ISSN = {1351-0347}, url = {http://dx.doi.org/10.1080/13510340802362646}, Abstract = {This article argues that constitutionalism and democratic institutionalization are linked, and that variations in progress towards institutionalized democracy are explained by incentives for political actors to comply with constitutional constraints on their power and to cooperate in governing. The analysis examines the impact of incentives generated by political institutions on Ecuador and Uruguay's contrasting experiences in institutionalizing democracy. Institutions generate incentives for political actors to 'play by the rules' when they extend protections, align interest with duty, and encourage negotiation and compromise. Survival provisions, electoral rules, and the nature of parties and the party system are found to generate incentives to cooperate in governing and to comply with constitutional constraints in Uruguay, and disincentives to engage in these behaviours in Ecuador. A new classification of survival provisions is proposed - shared, mixed, and separate - which isolates the impact of these rules on the degree of cooperation in governing. The article's findings clarify the mechanisms by which institutional choices facilitate or obstruct the emergence of constitutionalism and institutionalized democracy.}, Doi = {10.1080/13510340802362646}, Key = {fds227789} } @article{fds227827, Author = {Gesquiere, LR and Khan, M and Shek, L and Wango, EO and Alberts, SC and Altmann, J}, Title = {Coping with a challenging environment: seasonal variation in glucocorticoids in female baboons (Papio cynocephalus)}, Journal = {Hormones and Behavior}, Volume = {54}, Number = {3}, Pages = {410-416}, Year = {2008}, ISSN = {0018-506X}, url = {http://dx.doi.org/10.1016/j.yhbeh.2008.04.007}, Abstract = {Environmental stressors impact physiology and behavior in many species of animals. These effects are partly mediated through changing concentrations of glucocorticoids, which also vary with reproductive state and social conditions. Prior research has focused largely on seasonal breeders, but the close temporal linkage between season and reproductive state in these species hinders ability to disentangle environmental effects from those of the animal's reproductive status. Here we assessed the effects of environmental challenges on the fecal glucocorticoid (fGC) levels of non-seasonal breeders, female baboons (Papio cynocephalus) of Amboseli, Kenya. Amboseli is characterized by a long dry season, during which food and water become scarce, and by extreme temperatures above 40 °C in the shade during some months of the year. We found that after accounting for female reproductive status and individual variability, females exhibited higher fGC levels during the dry season than during the wet season. Further, during the wet season, fGC levels were higher in months of high average daily maximum temperatures. During the dry season, fGC levels were elevated both in hotter months and in months during which the baboons spent a relatively high proportion of time feeding. In spite of these stressors, female baboons reproduce during all months of the year in Amboseli, unlike most other mammals in this environment. This may be attributable to their extreme adaptability, specifically their diversified diet, and their ability to modify their behavior, including their activity profiles. © 2008 Elsevier Inc. All rights reserved.}, Doi = {10.1016/j.yhbeh.2008.04.007}, Key = {fds227827} } @article{fds227835, Author = {Charpentier, MJE and Widdig, A and Alberts, SC}, Title = {Inbreeding depression in non-human primates: a historical review of methods used and empirical data.}, Journal = {American journal of primatology}, Volume = {69}, Number = {12}, Pages = {1370-1386}, Year = {2007}, Month = {December}, ISSN = {0275-2565}, url = {http://www.ncbi.nlm.nih.gov/pubmed/17486606}, Abstract = {Offspring born to related parents may show reduced fitness due to inbreeding depression. Although evidence of inbreeding depression has accumulated for a variety of taxa during the past two decades, such analyses remain rare for primate species, probably because of their long generation time. However, inbreeding can have important fitness costs and is likely to shape life-history traits in all living species. As a consequence, selection should have favored inbreeding avoidance via sex-biased dispersal, extra-group paternity, or kin discrimination. In this paper, we review empirical studies on the effects of inbreeding on fitness traits or fitness correlates in primate species. In addition, we report the methods that have been used to detect inbreeding in primate populations, and their development with the improvement of laboratory techniques. We focus particularly on the advantages and disadvantages using microsatellite loci to detect inbreeding. Although the genetic data that are typically available (partial pedigrees, use of microsatellite heterozygosity as an estimate of genomewide inbreeding) tend to impose constraints on analyses, we encourage primatologists to explore the potential effects of inbreeding if they have access to even partial pedigrees or genetic information. Such studies are important because of both the value of basic research in inbreeding depression in the wild and the conservation issues associated with inbreeding, particularly in threatened species, which include more than half of the currently living primate species.}, Doi = {10.1002/ajp.20445}, Key = {fds227835} } @article{fds227837, Author = {Van Horn and RC and Buchan, JC and Altmann, J and Alberts, SC}, Title = {Divided destinies: Group choice by female savannah baboons during social group fission}, Journal = {Behavioral Ecology and Sociobiology}, Volume = {61}, Number = {12}, Pages = {1823-1837}, Publisher = {Springer Nature}, Year = {2007}, Month = {October}, ISSN = {0340-5443}, url = {http://dx.doi.org/10.1007/s00265-007-0415-1}, Abstract = {Group living provides benefits to individuals while imposing costs on them. In species that live in permanent social groups, group division provides the only opportunity for nondispersing individuals to change their group membership and improve their benefit to cost ratio. We examined group choice by 81 adult female savannah baboons (Papio cynocephalus) during four fission events. We measured how each female's group choice was affected by several factors: the presence of her maternal kin, paternal kin, age peers, and close social partners, her average kinship to groupmates, and her potential for improved dominance rank. Maternal kin, paternal kin, and close social partners influenced group choice by some females, but the relative importance of these factors varied across fissions. Age peers other than paternal kin had no effect on group choice, and average kinship to all groupmates had the same effect on group choice as did maternal kin alone. Most females were subordinate to fewer females after fissions than before, but status improvement did not drive female group choice; females often preferred to remain with social superiors who were their close maternal kin, rather than improving their own social ranks. We suggest that during permanent group fissions, female baboons prefer to remain with close maternal kin if those are abundant enough to influence their fitness; if they have too few close maternal kin then females prefer to remain with close paternal kin, and social bonds with nonkin might also become influential. © 2007 Springer-Verlag.}, Doi = {10.1007/s00265-007-0415-1}, Key = {fds227837} } @article{fds227838, Author = {Archie, EA and Hollister-Smith, JA and Poole, JH and Lee, PC and Moss, CJ and Maldonado, JE and Fleischer, RC and Alberts, SC}, Title = {Behavioural inbreeding avoidance in wild African elephants.}, Journal = {Molecular ecology}, Volume = {16}, Number = {19}, Pages = {4138-4148}, Year = {2007}, Month = {October}, ISSN = {0962-1083}, url = {http://dx.doi.org/10.1111/j.1365-294x.2007.03483.x}, Abstract = {The costs of inbreeding depression, as well as the opportunity costs of inbreeding avoidance, determine whether and which mechanisms of inbreeding avoidance evolve. In African elephants, sex-biased dispersal does not lead to the complete separation of male and female relatives, and so individuals may experience selection to recognize kin and avoid inbreeding. However, because estrous females are rare and male-male competition for mates is intense, the opportunity costs of inbreeding avoidance may be high, particularly for males. Here we combine 28 years of behavioural and demographic data on wild elephants with genotypes from 545 adult females, adult males, and calves in Amboseli National Park, Kenya, to test the hypothesis that elephants engage in sexual behaviour and reproduction with relatives less often than expected by chance. We found support for this hypothesis: males engaged in proportionally fewer sexual behaviours and sired proportionally fewer offspring with females that were natal family members or close genetic relatives (both maternal and paternal) than they did with nonkin. We discuss the relevance of these results for understanding the evolution of inbreeding avoidance and for elephant conservation.}, Doi = {10.1111/j.1365-294x.2007.03483.x}, Key = {fds227838} } @article{fds227834, Author = {Tung, J and Rudolph, J and Altmann, J and Alberts, SC}, Title = {Parallel effects of genetic variation in ACE activity in baboons and humans.}, Journal = {American journal of physical anthropology}, Volume = {134}, Number = {1}, Pages = {1-8}, Year = {2007}, Month = {September}, ISSN = {0002-9483}, url = {http://www.ncbi.nlm.nih.gov/pubmed/17503445}, Abstract = {Like humans, savannah baboons (Papio sp.) show heritable interindividual variation in complex physiological phenotypes. One prominent example of such variation involves production of the homeostatic regulator protein angiotensin converting enzyme (ACE), which shows heritable variation in both baboons and humans. In humans, this phenotypic variation is associated with an Alu insertion-deletion polymorphism in the ACE gene, which explains approximately half of the variation in serum ACE activity. We identified a similar Alu insertion-deletion polymorphism in the baboon ACE homologue and measured its frequency in a wild population and a captive population of baboons. We also analyzed the contribution of ACE genotype at this indel to variation in serum ACE activity in the captive population. When conditioned on weight, a known factor affecting ACE activity in humans, age and ACE genotype both accounted for variance in ACE activity; in particular, we identified a significant nonadditive interaction between age and genotype. A model incorporating this interaction effect explained 21.6% of the variation in residual serum ACE activity. Individuals homozygous for the deletion mutation exhibited significantly higher levels of ACE activity than insertion-deletion heterozygotes at younger ages (10-14 years), but showed a trend towards lower levels of ACE activity compared with heterozygotes at older ages (> or =15 years). These results demonstrate an interesting parallel between the genetic architecture underlying ACE variation in humans and baboons, suggesting that further attention should be paid in humans to the relationship between ACE genetic variation and aging.}, Doi = {10.1002/ajpa.20614}, Key = {fds227834} } @article{fds304244, Author = {Hollister-Smith, JA and Poole, JH and Archie, EA and Vance, EA and Georgiadis, NJ and Moss, CJ and Alberts, SC}, Title = {Age, musth and paternity success in wild male African elephants, Loxodonta africana}, Journal = {Animal Behaviour}, Volume = {74}, Number = {2}, Pages = {287-296}, Publisher = {Elsevier BV}, Year = {2007}, Month = {August}, ISSN = {0003-3472}, url = {http://dx.doi.org/10.1016/j.anbehav.2006.12.008}, Abstract = {Male African elephants experience intense intrasexual selection in gaining access to oestrous females, who represent a very scarce and highly mobile resource. An unusual combination of behavioural and physiological traits in males probably reflects this intense selection pressure. Males show prolonged growth, growing throughout much or perhaps all of their long life span (ca. 60-65 years), and they show musth, a physiological and behavioural condition exclusive to elephants, which is manifested by bouts of elevated testosterone and aggression and heightened sexual activity. Most observed matings are by males over 35 years of age and in musth, suggesting that age and musth are both important factors contributing to male reproductive success. Here we report the results of a genetic paternity analysis of a well-studied population of wild African elephants. Patterns of paternity for 119 calves born over a 22-year period showed significant effects of both age and musth on paternity success. Among males in musth, paternity success increased significantly with age until the very oldest age classes, when it modestly declined. When not in musth, males experienced relatively constant, low levels of paternity success at all ages. Thus, despite the importance of both musth and age in determining male paternity success, adult males both in and out of musth, and of all ages, produced calves. In general, however, older males had markedly elevated paternity success compared with younger males, suggesting the possibility of sexual selection for longevity in this species. © 2007 The Association for the Study of Animal Behaviour.}, Doi = {10.1016/j.anbehav.2006.12.008}, Key = {fds304244} } @article{fds227846, Author = {Gesquiere, LR and Wango, EO and Alberts, SC and Altmann, J}, Title = {Mechanisms of sexual selection: sexual swellings and estrogen concentrations as fertility indicators and cues for male consort decisions in wild baboons.}, Journal = {Hormones and behavior}, Volume = {51}, Number = {1}, Pages = {114-125}, Year = {2007}, Month = {January}, ISSN = {0018-506X}, url = {http://dx.doi.org/10.1016/j.yhbeh.2006.08.010}, Abstract = {Male mate-guarding episodes ('consortships'), are taxonomically widespread, yet costly to individual males. Consequently, males should bias consortships toward females with whom the probability of conception is high. We combined data on consortships with visual scoring of sexual swellings and assays of fecal estrogen concentrations (fE) in a wild population of baboons (Papio cynocephalus) to test the hypotheses that sexual swellings are reliable indicators of (1) within-cycle timing of ovulation, (2) differences in conception probability among females that differ in maturational stage, and (3) conceptive versus non-conceptive cycles of parous females. We also evaluated whether adult males might rely on swellings or other estrogen-dependent signals (e.g., fE) for mate-guarding decisions. We found that sexual swellings reflected conception probability within and among cycles. Adult males limited their consortships to the turgescent phase of cycles, and consorted more with adult females than with newly cycling adolescents. The highest ranking (alpha) males discriminated more than did males of other ranks; they (1) limited their consortships to the 5-day peri-ovulatory period, (2) consorted more with adult than with adolescent females, and (3) consorted more with adult females on conceptive cycles than on non-conceptive cycles, all to a greater extent than did males of other ranks. Male mate choice based on sexual swellings and other estrogenic cues of fertility may result in sexual selection on these female traits and enhance dominance-based reproductive skew in males. Alpha males are the least constrained in their mating behavior and can best take advantage of these cues to mate selectively.}, Doi = {10.1016/j.yhbeh.2006.08.010}, Key = {fds227846} } @article{fds227836, Author = {Hollister Smith and JA and Poole, JH and Archie, EA and Vance, EA and Georgiadis, NJ and Moss, CJ and Alberts, SC}, Title = {Paternity success in wild African elephants}, Journal = {Animal Behaviour}, Volume = {74}, Number = {2}, Pages = {287-296}, Year = {2007}, ISSN = {0003-3472}, url = {http://dx.doi.org/10.1016/j.anbehav.2006.12.008}, Abstract = {Male African elephants experience intense intrasexual selection in gaining access to oestrous females, who represent a very scarce and highly mobile resource. An unusual combination of behavioural and physiological traits in males probably reflects this intense selection pressure. Males show prolonged growth, growing throughout much or perhaps all of their long life span (ca. 60-65 years), and they show musth, a physiological and behavioural condition exclusive to elephants, which is manifested by bouts of elevated testosterone and aggression and heightened sexual activity. Most observed matings are by males over 35 years of age and in musth, suggesting that age and musth are both important factors contributing to male reproductive success. Here we report the results of a genetic paternity analysis of a well-studied population of wild African elephants. Patterns of paternity for 119 calves born over a 22-year period showed significant effects of both age and musth on paternity success. Among males in musth, paternity success increased significantly with age until the very oldest age classes, when it modestly declined. When not in musth, males experienced relatively constant, low levels of paternity success at all ages. Thus, despite the importance of both musth and age in determining male paternity success, adult males both in and out of musth, and of all ages, produced calves. In general, however, older males had markedly elevated paternity success compared with younger males, suggesting the possibility of sexual selection for longevity in this species. © 2007 The Association for the Study of Animal Behaviour.}, Doi = {10.1016/j.anbehav.2006.12.008}, Key = {fds227836} } @article{fds227841, Author = {Silk, JB and Altmann, J and Alberts, SC}, Title = {Social relationships among adult female baboons (papio cynocephalus) I. Variation in the strength of social bonds}, Journal = {Behavioral Ecology and Sociobiology}, Volume = {61}, Number = {2}, Pages = {183-195}, Publisher = {Springer Nature}, Year = {2006}, Month = {December}, ISSN = {0340-5443}, url = {http://dx.doi.org/10.1007/s00265-006-0249-2}, Abstract = {Sociality has positive effects on female fitness in many mammalian species. Among female baboons, those who are most socially integrated reproduce most successfully. Here we test a number of predictions derived from kin selection theory about the strength of social bonds among adult female baboons. Our analyses are based on systematic observations of grooming and association patterns among 118 females living in seven different social groups in the Amboseli Basin of Kenya over a 16-year period. Females in these groups formed the strongest bonds with close kin, including their mothers, daughters, and maternal and paternal sisters. Females were also strongly attracted toward females who were close to their own age, perhaps because peers were often paternal sisters. Females' bonds with their maternal sisters were strengthened after their mother's deaths, whereas their relationships with their maternal aunts were weakened after their mother's death. In addition, females formed stronger bonds with their paternal sisters when no close maternal kin were available, and they compensated for the absence of any close kin by forming strong bonds with nonrelatives. Taken together, these data suggest that social bonds play a vital role in females' lives, and the ability to establish and maintain strong social bonds may have important fitness consequences for females. © 2006 Springer-Verlag.}, Doi = {10.1007/s00265-006-0249-2}, Key = {fds227841} } @article{fds227842, Author = {Silk, JB and Alberts, SC and Altmann, J}, Title = {Social relationships among adult female baboons (Papio cynocephalus) II. Variation in the quality and stability of social bonds}, Journal = {Behavioral Ecology and Sociobiology}, Volume = {61}, Number = {2}, Pages = {197-204}, Publisher = {Springer Nature}, Year = {2006}, Month = {December}, ISSN = {0340-5443}, url = {http://dx.doi.org/10.1007/s00265-006-0250-9}, Abstract = {A growing body of evidence suggests that social bonds have adaptive value for animals that live in social groups. Although these findings suggest that natural selection may favor the ability to cultivate and sustain social bonds, we know very little about the factors that influence the quality or stability of social bonds. Here, we draw on data derived from a 16-year study of baboons living in seven different social groups in the Amboseli basin of Kenya to evaluate the quality and stability of social bonds among females. Our results extend previous analyses, which demonstrate that females form the strongest bonds with close maternal and paternal kin, age mates (who may be paternal kin), and females who occupy similar ranks but are not maternal relatives. Here we show that the same factors influence the quality and strength of social bonds. Moreover, the results demonstrate that the quality of social bonds directly affects their stability. © 2006 Springer-Verlag.}, Doi = {10.1007/s00265-006-0250-9}, Key = {fds227842} } @article{fds227843, Author = {Alberts, SC and Buchan, JC and Altmann, J}, Title = {Sexual selection in wild baboons: from mating opportunities to paternity success}, Journal = {Animal Behaviour}, Volume = {72}, Number = {5}, Pages = {1177-1196}, Publisher = {Elsevier BV}, Year = {2006}, Month = {November}, ISSN = {0003-3472}, url = {http://dx.doi.org/10.1016/j.anbehav.2006.05.001}, Abstract = {In mammals, high dominance rank among males is often associated with mating success. However, mating opportunities do not automatically translate into offspring production; observed mating success may be discordant with offspring production, for three reasons. (1) Observed mating may be nonrepresentative of actual mating if some mating is surreptitious (decreasing the chance that it will be observed), (2) mating may be nonrandom if some males allocate more mating effort to females with high fertility (i.e. if some males differentially invest in higher fertility mating) and (3) conception success may be nonrandom if sperm competition or sperm selection play a role in conception. We performed a genetic analysis of paternity in the well-studied savannah baboon, Papio cynocephalus, population in the Amboseli basin, eastern Africa, in order to measure the concordance between observed mating success and actual offspring production. We found that observed mating success was generally a good predictor of paternity success, that high-ranking males had higher paternity success than lower-ranking males, and that male density and male rank stability contributed to variance in male paternity success. We found little evidence for successful surreptitious mating (although subadult males did occasionally produce offspring, apparently using this strategy), and no clear evidence for differential sperm success or sperm depletion (although we could not rule them out). However, we found clear evidence that high-ranking males showed mate choice, concentrating their mating efforts on females experiencing conceptive rather than nonconceptive cycles. © 2006 The Association for the Study of Animal Behaviour.}, Doi = {10.1016/j.anbehav.2006.05.001}, Key = {fds227843} } @article{fds227839, Author = {Loisel, DA and Rockman, MV and Wray, GA and Altmann, J and Alberts, SC}, Title = {Ancient polymorphism and functional variation in the primate MHC-DQA1 5' cis-regulatory region.}, Journal = {Proceedings of the National Academy of Sciences of the United States of America}, Volume = {103}, Number = {44}, Pages = {16331-16336}, Year = {2006}, Month = {October}, ISSN = {0027-8424}, url = {http://www.ncbi.nlm.nih.gov/pubmed/17053068}, Abstract = {Precise regulation of MHC gene expression is critical to vertebrate immune surveillance and response. Polymorphisms in the 5' proximal promoter region of the human class II gene HLA-DQA1 have been shown to influence its transcriptional regulation and may contribute to the pathogenesis of autoimmune diseases. We investigated the evolutionary history of this cis-regulatory region by sequencing the DQA1 5' proximal promoter region in eight nonhuman primate species. We observed unexpectedly high levels of sequence variation and multiple strong signatures of balancing selection in this region. Specifically, the considerable DQA1 promoter region diversity was characterized by abundant shared (or trans-species) polymorphism and a pronounced lack of fixed differences between species. The majority of transcription factor binding sites in the DQA1 promoter region were polymorphic within species, and these binding site polymorphisms were commonly shared among multiple species despite evidence for negative selection eliminating a significant fraction of binding site mutations. We assessed the functional consequences of intraspecific promoter region diversity using a cell line-based reporter assay and detected significant differences among baboon DQA1 promoter haplotypes in their ability to drive transcription in vitro. The functional differentiation of baboon promoter haplotypes, together with the significant deviations from neutral sequence evolution, suggests a role for balancing selection in the evolution of DQA1 transcriptional regulation in primates.}, Doi = {10.1073/pnas.0607662103}, Key = {fds227839} } @article{fds227845, Author = {Beehner, JC and Onderdonk, DA and Alberts, SC and Altmann, J}, Title = {The ecology of conception and pregnancy failure in wild baboons}, Journal = {Behavioral Ecology}, Volume = {17}, Number = {5}, Pages = {741-750}, Publisher = {Oxford University Press (OUP)}, Year = {2006}, Month = {September}, ISSN = {1045-2249}, url = {http://dx.doi.org/10.1093/beheco/arl006}, Abstract = {Environmental conditions are a key factor mediating reproductive success or failure. Consequently, many mammalian taxa have breeding seasons that coordinate critical reproductive stages with optimal environmental conditions. However, in contrast with most mammals, baboons (Papio cynocephalus) of Kenya reproduce throughout the year. Here we depart from the typical approach of evaluating seasonal effects on reproduction and engage in a more fine-grained analysis of the actual ecological conditions leading up to reproduction for females. Our aim was to determine how environmental conditions, in combination with social and demographic factors, might mediate baboon reproduction. The data set includes all female reproductive cycles from multiple baboon groups in the Amboseli basin between 1976 and 2004. Results indicate that after periods of drought or extreme heat, females were significantly less likely to cycle than expected. If females did cycle after these conditions, they were less likely to conceive; and if they did conceive after drought (heat effects were nonsignificant), they were less likely to have a successful pregnancy. Age also significantly predicted conceptive failure; conceptive probability was lowest among the youngest and oldest cycling females. There was also a trend for high ambient temperatures to contribute to fetal loss during the first trimester but not other trimesters. Finally, group size and drought conditions interacted in their effects on the probability of conception. Although females in all groups had equal conception probabilities during optimal conditions, females in large groups were less likely than those in small groups to conceive during periods of drought. These results indicate that in a highly variable environment, baboon reproductive success is mediated by the interaction between proximate ecological conditions and individual demographic factors. © The Author 2006. Published by Oxford University Press on behalf of the International Society for Behavioral Ecology. All rights reserved.}, Doi = {10.1093/beheco/arl006}, Key = {fds227845} } @article{fds227840, Author = {Beehner, JC and Nguyen, N and Wango, EO and Alberts, SC and Altmann, J}, Title = {The endocrinology of pregnancy and fetal loss in wild baboons.}, Journal = {Hormones and behavior}, Volume = {49}, Number = {5}, Pages = {688-699}, Year = {2006}, Month = {May}, ISSN = {0018-506X}, url = {http://dx.doi.org/10.1016/j.yhbeh.2005.12.016}, Abstract = {An impressive body of research has focused on the mechanisms by which the steroid estrogens (E), progestins (P), and glucocorticoids (GC) ensure successful pregnancy. With the advance of non-invasive techniques to measure steroids in urine and feces, steroid hormones are routinely monitored to detect pregnancy in wild mammalian species, but hormone data on fetal loss have been sparse. Here, we examine fecal steroid hormones from five groups of wild yellow baboons (Papio cynocephalus) in the Amboseli basin of Kenya to compare the hormones of successful pregnancies to those ending in fetal loss or stillbirth. Using a combination of longitudinal and cross-sectional data, we analyzed three steroid hormones (E, P, GC) and related metabolites from 5 years of fecal samples across 188 pregnancies. Our results document the course of steroid hormone concentrations across successful baboon pregnancy in the wild and demonstrate that fecal estrogens predicted impending fetal loss starting 2 months before the externally observed loss. By also considering an additional 450 pregnancies for which we did not have hormonal data, we determined that the probability for fetal loss for Amboseli baboons was 13.9%, and that fetal mortality occurred throughout gestation (91 losses occurred in 656 pregnancies; rates were the same for pregnancies with and without hormonal data). These results demonstrate that our longstanding method for early detection of pregnancies based on observation of external indicators closely matches hormonal identification of pregnancy in wild baboons.}, Doi = {10.1016/j.yhbeh.2005.12.016}, Key = {fds227840} } @article{fds227847, Author = {Archie, EA and Moss, CJ and Alberts, SC}, Title = {The ties that bind: genetic relatedness predicts the fission and fusion of social groups in wild African elephants.}, Journal = {Proceedings. Biological sciences}, Volume = {273}, Number = {1586}, Pages = {513-522}, Year = {2006}, Month = {March}, ISSN = {0962-8452}, url = {http://www.ncbi.nlm.nih.gov/pubmed/16537121}, Abstract = {Many social animals live in stable groups. In contrast, African savannah elephants (Loxodonta africana) live in unusually fluid, fission-fusion societies. That is, 'core' social groups are composed of predictable sets of individuals; however, over the course of hours or days, these groups may temporarily divide and reunite, or they may fuse with other social groups to form much larger social units. Here, we test the hypothesis that genetic relatedness predicts patterns of group fission and fusion among wild, female African elephants. Our study of a single Kenyan population spans 236 individuals in 45 core social groups, genotyped at 11 microsatellite and one mitochondrial DNA (mtDNA) locus. We found that genetic relatedness predicted group fission; adult females remained with their first order maternal relatives when core groups fissioned temporarily. Relatedness also predicted temporary fusion between social groups; core groups were more likely to fuse with each other when the oldest females in each group were genetic relatives. Groups that shared mtDNA haplotypes were also significantly more likely to fuse than groups that did not share mtDNA. Our results suggest that associations between core social groups persist for decades after the original maternal kin have died. We discuss these results in the context of kin selection and its possible role in the evolution of elephant sociality.}, Doi = {10.1098/rspb.2005.3361}, Key = {fds227847} } @article{fds304243, Author = {Archie, EA and Morrison, TA and Foley, CAH and Moss, CJ and Alberts, SC}, Title = {Dominance rank relationships among wild female African elephants, Loxodonta africana}, Journal = {Animal Behaviour}, Volume = {71}, Number = {1}, Pages = {117-127}, Publisher = {Elsevier BV}, Year = {2006}, Month = {January}, ISSN = {0003-3472}, url = {http://dx.doi.org/10.1016/j.anbehav.2005.03.023}, Abstract = {Socioecological models of the evolution of female-bonded societies predict a relation between resource distribution and the nature of female affiliative and dominance relationships. Species that mainly rely on abundant, widely distributed resources, like African savanna elephants, are predicted to have unresolved dominance hierarchies and poorly differentiated female social relationships. Contrary to this prediction, female elephants have well-differentiated social relationships; however, little is known about the nature of their dominance rank relationships. Here we present the first quantitative analysis of dominance relationships within 'family' groups of adult female elephants in two wild populations: one in Amboseli National Park, Kenya, and another in Tarangire National Park, Tanzania. We tested three possibilities, that female elephants: (1) are egalitarian, (2) have linear, nepotistic hierarchies, or (3) have linear age/size-ordered hierarchies. Our results best support the third outcome: dominance rank relationships were transitive within families and highly asymmetrical within dyads, such that older, larger females consistently dominated smaller, younger females. We discuss the implications of this result for understanding the evolution of female social relationships. © 2005 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.}, Doi = {10.1016/j.anbehav.2005.03.023}, Key = {fds304243} } @article{fds227844, Author = {Archie, EA and Morrison, TA and Foley, CA and Moss, CJ and Alberts, SC}, Title = {Linear dominance hierarchies in African elephants}, Journal = {Animal Behaviour}, Volume = {71}, Number = {1}, Pages = {117-127}, Year = {2006}, ISSN = {0003-3472}, url = {http://dx.doi.org/10.1016/j.anbehav.2005.03.023}, Abstract = {Socioecological models of the evolution of female-bonded societies predict a relation between resource distribution and the nature of female affiliative and dominance relationships. Species that mainly rely on abundant, widely distributed resources, like African savanna elephants, are predicted to have unresolved dominance hierarchies and poorly differentiated female social relationships. Contrary to this prediction, female elephants have well-differentiated social relationships; however, little is known about the nature of their dominance rank relationships. Here we present the first quantitative analysis of dominance relationships within 'family' groups of adult female elephants in two wild populations: one in Amboseli National Park, Kenya, and another in Tarangire National Park, Tanzania. We tested three possibilities, that female elephants: (1) are egalitarian, (2) have linear, nepotistic hierarchies, or (3) have linear age/size-ordered hierarchies. Our results best support the third outcome: dominance rank relationships were transitive within families and highly asymmetrical within dyads, such that older, larger females consistently dominated smaller, younger females. We discuss the implications of this result for understanding the evolution of female social relationships. © 2005 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.}, Doi = {10.1016/j.anbehav.2005.03.023}, Key = {fds227844} } @article{fds227778, Author = {Buchan, JC and Archie, EA and Van Horn and RC and Moss, CJ and Alberts, SC}, Title = {Locus effects and sources of error in noninvasive genotyping}, Journal = {Molecular Ecology Notes}, Volume = {5}, Number = {3}, Pages = {680-683}, Publisher = {WILEY}, Year = {2005}, Month = {September}, ISSN = {1471-8278}, url = {http://dx.doi.org/10.1111/j.1471-8286.2005.01002.x}, Abstract = {In spite of more than a decade of research on noninvasive genetic sampling, the low quality and quantity of DNA in noninvasive studies continue to plague researchers. Effects of locus size on error have been documented but are still poorly understood. Further, sources of error other than allelic dropout have been described but are often not well quantified. Here we analyse the effects of locus size on allelic dropout, amplification success and error rates in noninvasive genotyping studies of three species, and quantify error other than allelic dropout. © 2005 Blackwell Publishing Ltd.}, Doi = {10.1111/j.1471-8286.2005.01002.x}, Key = {fds227778} } @article{fds227858, Author = {Morrison, TA and Chiyo, PI and Moss, CJ and Alberts, SC}, Title = {Measures of dung bolus size for known-age African elephants (Loxodonta africana): Implications for age estimation}, Journal = {Journal of Zoology}, Volume = {266}, Number = {1}, Pages = {89-94}, Publisher = {WILEY}, Year = {2005}, Month = {May}, url = {http://dx.doi.org/10.1017/S0952836905006631}, Abstract = {The availability of a population of mostly known-age African elephants Loxodonta africana from Amboseli National Park, Kenya, provided a unique opportunity to assess the use of dung bolus diameter for estimating age. A predictive equation for estimating dung bolus diameters from elephants of known age was derived and was found to follow the typical growth pattern exhibited by changes in shoulder height and foot length. The relationship between measurements of dung bolus and age was particularly strong when growth rates were high (age 0-25 years). The dung bolus growth curve from Amboseli elephants was similar to that derived from another wild population of African elephants, suggesting that dung bolus diameter can be used to assess age structure in areas where it is impossible to construct independent prediction curves of age and dung bolus. © 2005 The Zoological Society of London.}, Doi = {10.1017/S0952836905006631}, Key = {fds227858} } @article{fds227857, Author = {Altmann, J and Alberts, SC}, Title = {Growth rates in a wild primate population: Ecological influences and maternal effects}, Journal = {Behavioral Ecology and Sociobiology}, Volume = {57}, Number = {5}, Pages = {490-501}, Publisher = {Springer Nature}, Year = {2005}, Month = {March}, url = {http://dx.doi.org/10.1007/s00265-004-0870-x}, Abstract = {Growth rate is a life-history trait often linked to various fitness components, including survival, age of first reproduction, and fecundity. Here we present an analysis of growth-rate variability in a wild population of savannah baboons (Papio cynocephalus). We found that relative juvenile size was a stable individual trait during the juvenile period: individuals generally remained consistently large-for-age or small-for-age throughout development. Resource availability, which varied greatly in the study population (between completely wild-foraging and partially food-enhanced social groups), had major effects on growth. Sexual maturity was accelerated for animals in the food-enhanced foraging condition, and the extent and ontogeny of sexual dimorphism differed with resource availability. Maternal characteristics also had significant effects on growth. Under both foraging conditions, females of high dominance rank and multiparous females had relatively large-for-age juveniles. Large relative juvenile size predicted earlier age of sexual maturation for both males and females in the wild-feeding condition. This confirmed that maternal effects were pervasive and contributed to differences among individuals in fitness components. © Springer-Verlag 2004.}, Doi = {10.1007/s00265-004-0870-x}, Key = {fds227857} } @article{fds227848, Author = {Gesquiere, LR and Altmann, J and Khan, MZ and Couret, J and Yu, JC and Endres, CS and Lynch, JW and Ogola, P and Fox, EA and Alberts, SC and Wango, E}, Title = {Coming of age: steroid hormones of wild immature baboons, Papio cynocephalus}, Journal = {American Journal of Primatology}, Volume = {67}, Number = {1}, Pages = {83-100}, Year = {2005}, ISSN = {0275-2565}, url = {http://dx.doi.org/10.1002/ajp.20171}, Abstract = {Large gaps exist in our knowledge about common patterns and variability in the endocrinology of immature nonhuman primates, and even normal hormonal profiles during that life stage are lacking for wild populations. In the present study we present steroid profiles for a wild population of baboons (Papio cynocephalus) from infancy through reproductive maturation, obtained by noninvasive fecal analyses. Fecal concentrations of glucocorticoid (fGC) and testosterone (fT) metabolites for males, and of fGC, estrogen (fE), and progestin (fP) metabolites for females were measured by radioimmunoassay (RIA). In males, infancy was characterized by high and declining levels of fGC and fT, whereas steroid concentrations were low during the juvenile years. During the months immediately prior to testicular enlargement, fT (but not fGC) concentration tended to increase. Males that matured early consistently had higher fT and fGC concentrations than those that matured late, but not significantly so at any age. Individual differences in fT concentrations were stable across ages, and average individual fT and fGC concentrations were positively correlated. For females, high and declining levels of fE characterized infancy, and values increased again after 3.5 years of age, as some females reached menarche by that age. Both fP and fGC were relatively low and constant throughout infancy and the juvenile period. During the months immediately prior to menarche, fGC concentration significantly decreased, while no changes were observed for fE levels. fP exhibited a complicated pattern of decrease that was subsequently followed by a more modest and nonsignificant increase as menarche approached. Early- (EM) and late-maturing (LM) females differed only in fP concentration; the higher fP concentrations in EM females reached significance at 4-4.5 years of age. Maternal rank at offspring conception did not predict concentrations of any hormone for either sex. Our results demonstrate the presence of individual endocrine variability, which could have important consequences for the timing of sexual maturation and subsequently for individual reproductive success. Further evaluation of the factors that affect hormone concentrations during the juvenile and adolescent periods should lead to a better understanding of mechanisms of life-history variability.}, Doi = {10.1002/ajp.20171}, Key = {fds227848} } @article{fds227856, Author = {Altmann, J and Lynch, JW and Nguyen, N and Alberts, SC and Gesquiere, LR}, Title = {Life-history correlates of steroid concentrations in wild peripartum baboons.}, Journal = {American journal of primatology}, Volume = {64}, Number = {1}, Pages = {95-106}, Year = {2004}, Month = {September}, url = {http://dx.doi.org/10.1002/ajp.20064}, Abstract = {Steroid concentrations during late pregnancy and early lactation may be affected by both a female's reproductive history and her current condition, and may in turn predict subsequent life-history events, such as offspring survival. This study investigated these relationships in a wild primate population through the use of fecal steroid analysis in repeated sampling of peripartum baboons (Papio cynocephalus). Fecal samples were collected from 32 females in five groups within the Amboseli basin during 8 weeks prior to parturition and 13 weeks postpartum. From December 1999 through February 2002, 176 fecal samples were collected from individuals representing 39 peripartum periods. Fecal concentrations of progestins (fP), estrogen metabolites (fE), glucocorticoids (fGC), and testosterone metabolites (fT) were measured by radioimmunoassay. Steroid concentrations declined from late pregnancy to lactation, and the decline was greatest and most precipitous for fE and fP. Primiparous females had significantly higher mean fE concentrations in each of the last 2 months of pregnancy compared to multiparous females. Among multiparous females, fE and fT were significantly higher during late pregnancy in females carrying a male fetus compared to those carrying a female fetus. During early lactation, high fT in young mothers predicted subsequent infant death during the first year of life. These findings illustrate the potential power of repeated fecal-steroid sampling to elucidate mechanisms of life-history variability in natural populations. They also document significant differences in hormone profiles among subgroups, and highlight that such normative subgroup information is essential for interpreting individual variability in hormone-behavior associations.}, Doi = {10.1002/ajp.20064}, Key = {fds227856} } @article{fds227776, Author = {Alberts, SC and Altmann, J}, Title = {Reproductive behavior in wild baboons.}, Journal = {Gynecologic and obstetric investigation}, Volume = {57}, Number = {1}, Pages = {10-13}, Year = {2004}, Month = {January}, ISSN = {0378-7346}, url = {http://www.ncbi.nlm.nih.gov/pubmed/14971413}, Doi = {10.1159/000077385}, Key = {fds227776} } @article{fds227777, Author = {Silk, JB and Alberts, SC and Altmann, J}, Title = {Patterns of coalition formation by adult female baboons in Amboseli, Kenya}, Journal = {Animal Behaviour}, Volume = {67}, Number = {3}, Pages = {573-582}, Publisher = {Elsevier BV}, Year = {2004}, Month = {January}, ISSN = {0003-3472}, url = {http://dx.doi.org/10.1016/j.anbehav.2003.07.001}, Abstract = {Coalitionary support in agonistic interactions is generally thought to be costly to the actor and beneficial to the recipient. Explanations for such cooperative interactions usually invoke kin selection, reciprocal altruism or mutualism. We evaluated the role of these factors and individual benefits in shaping the pattern of coalitionary activity among adult female savannah baboons, Papio cynocephalus, in Amboseli, Kenya. There is a broad consensus that, when ecological conditions favour collective defence of resources, selection favours investment in social relationships with those likely to provide coalitionary support. The primary features of social organization in female-bonded groups, including female philopatry, linear dominance hierarchies, acquisition of maternal rank and well-differentiated female relationships, are thought to be functionally linked to the existence of alliances between females. Female savannah baboons display these characteristics, but the frequency and function of their coalitionary aggression is disputed. In our five study groups, 4-6% of all disputes between females led to intervention by third parties. Adult females selectively supported close maternal kin. There was no evidence that females traded grooming for support or reciprocated support with nonkin. High-ranking females participated in coalitionary aggression most frequently, perhaps because they derived more benefits from group membership than other females did or could provide support at lower cost. Females typically supported the higher ranking of two contestants when they intervened in disputes between subordinates, so most coalitions reinforced the existing dominance hierarchy. Results indicate that female baboons participate in coalitionary aggression in a manner strongly influenced by nepotism and individual benefits. © 2004 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.}, Doi = {10.1016/j.anbehav.2003.07.001}, Key = {fds227777} } @article{fds227867, Author = {Silk, JB and Alberts, SC and Altmann, J}, Title = {Social bonds of female baboons enhance infant survival.}, Journal = {Science (New York, N.Y.)}, Volume = {302}, Number = {5648}, Pages = {1231-1234}, Year = {2003}, Month = {November}, url = {hgvj,hbklnkjhn;iohuiguyvgbjknbliub}, Abstract = {Among nonhuman primates, females often form strong bonds with kin and other group members. These relationships are thought to have adaptive value for females, but direct effects of sociality on fitness have never been demonstrated. We present 16 years of behavioral data from a well-studied population of wild baboons, which demonstrate that sociality of adult females is positively associated with infant survival, an important component of variation in female lifetime fitness. The effects of sociality on infant survival are independent of the effects of dominance rank, group membership, and environmental conditions. Our results are consistent with the evidence that social support has beneficial effects on human health and well-being across the life span. For humans and other primates, sociality has adaptive value.}, Doi = {10.1126/science.1088580}, Key = {fds227867} } @article{fds227850, Author = {Buchan, JC and Alberts, SC and Silk, JB and Altmann, J}, Title = {True paternal care in a multi-male primate society.}, Journal = {Nature}, Volume = {425}, Number = {6954}, Pages = {179-181}, Year = {2003}, Month = {September}, url = {http://www.ncbi.nlm.nih.gov/pubmed/12968180}, Abstract = {Although male parental care is rare among mammals, adult males of many cercopithecine primate species provide care for infants and juveniles. This care is often in the form of grooming, carrying, support in agonistic interactions, and protection against infanticide. For these behaviours to be interpreted as true parental care, males must selectively direct care towards their own offspring and this care must result in fitness benefits. With the exception of males defending probable offspring from infanticide, male primates living in multi-male, multi-female social groups have not been shown to selectively direct care towards their own offspring. We determined paternity for 75 juveniles in a population of wild savannah baboons (Papio cynocephalus) and collected data on interventions in agonistic disputes by adult males on behalf of juveniles as a form of male care. Here we show that adult males differentiate their offspring from unrelated juveniles and selectively support their offspring in agonistic disputes. As support in agonistic disputes is likely to contribute to rank acquisition and protect juveniles from injury and stress, this can be considered true parental care.}, Doi = {10.1038/nature01866}, Key = {fds227850} } @article{fds227882, Author = {Archie, EA and Moss, CJ and Alberts, SC}, Title = {Characterization of tetranucleotide microsatellite loci in the African Savannah Elephant (Loxodonta africana africana)}, Journal = {Molecular Ecology Notes}, Volume = {3}, Number = {2}, Pages = {244-246}, Publisher = {WILEY}, Year = {2003}, Month = {June}, url = {http://dx.doi.org/10.1046/j.1471-8286.2003.00412.x}, Abstract = {Most African elephant (Loxodonta africana africana) populations are isolated and thus threatened by a loss of genetic diversity. As a consequence, genetic analysis of African elephant populations will play an increasing role in their conservation, and microsatellite loci will be an important tool in these analyses. Previously published sets of polymorphic microsatellites developed for African elephants are all dinucleotide repeats, which are prone to typing error. Here, we characterize 11 tetranucleotide microsatellite loci in the African elephant. All loci were polymorphic in 32 faecal samples and two tissue samples from 33 individual African savannah elephants.}, Doi = {10.1046/j.1471-8286.2003.00412.x}, Key = {fds227882} } @article{fds227854, Author = {Altmann, J and Alberts, SC}, Title = {Variability in reproductive success viewed from a life-history perspective in baboons.}, Journal = {American journal of human biology : the official journal of the Human Biology Council}, Volume = {15}, Number = {3}, Pages = {401-409}, Year = {2003}, Month = {May}, url = {http://dx.doi.org/10.1002/ajhb.10157}, Abstract = {Nonhuman primates, like humans, mature slowly and have low fertility during a relatively long life. As data have accumulated on life-history patterns of nonhuman primates, comparative studies have yielded important insights into the evolution of this slow life-history style of primates. However, in order to understand selection pressures and evolutionary potential within species, it is important to complement comparative studies with detailed studies of life-history variability within species and to identify sources of this variability. Here we present a summary of how foraging environment, social status, and group size (a measure of population density) contribute to within-population variance in reproductive success for savannah baboons. We also discuss the extent to which savannah baboons, with their highly flexible and adaptable behavior, change their foraging environments by shifting home ranges and seeking rich food sources and how low-ranking females, which disproportionately bear the costs of social life, may mitigate those costs.}, Doi = {10.1002/ajhb.10157}, Key = {fds227854} } @article{fds227853, Author = {Hahn, NE and Proulx, D and Muruthi, PM and Alberts, S and Altmann, J}, Title = {Gastrointestinal parasites in free-ranging Kenyan baboons (Papio cynocephalus and P. anubis)}, Journal = {International Journal of Primatology}, Volume = {24}, Number = {2}, Pages = {271-279}, Year = {2003}, Month = {April}, url = {http://dx.doi.org/10.1023/A:1023092915171}, Abstract = {We screened fecal samples from 3 groups of wild-living baboons (Papio cynocephalus and P. anubis), involved in longitudinal behavioral studies, for evidence of gastrointestinal parasites. The two objectives of the study were: 1) to compare parasites from two of the groups with different foraging behavior from the same area and 2) to obtain fecal parasitic data on 3 groups of baboons to provide baseline reference data. We sampled individual baboons opportunistically from Lodge and Hook's groups, Amboseli National Park and from Mpala Group, Mpala Wildlife Research Centre, Kenya, Lodge Group baboons supplemented foraging on wild foods by daily foraging in human-source refuse, whereas Hook's and Mpala groups did not. We collected fecal samples from 55, 30 and 42 individuals in Hook's, Lodge and Mpala groups, respectively, and processed them via ether sedimentation. We identified strongylids, Streptopharagus sp., Physaloptera sp., Trichuris sp., Enterobius sp., and Strongyloides sp., in the feces, but no parasite directly attributable to exposure to people. Garbage- and wild-feeding Amboseli baboons differed in the prevalence of Streptopharagus sp., Physaloptera sp. and Trichuris sp.}, Doi = {10.1023/A:1023092915171}, Key = {fds227853} } @article{fds304242, Author = {Alberts, SC and Watts, HE and Altmann, J}, Title = {Queuing and queue-jumping: Long-term patterns of reproductive skew in male savannah baboons, Papio cynocephalus}, Journal = {Animal Behaviour}, Volume = {65}, Number = {4}, Pages = {821-840}, Publisher = {Elsevier BV}, Year = {2003}, Month = {April}, url = {http://dx.doi.org/10.1006/anbe.2003.2106}, Abstract = {In many animals, variance in male mating success is strongly correlated with male dominance rank or some other measure of fighting ability. Studies in primates, however, have varied greatly in whether they detect a relationship between male dominance rank and mating success. This variability has led to debate about the nature of the relation between rank and mating success in male primates. We contribute to the resolution of this debate by presenting an analysis of the relationship between dominance rank and male mating success over 32 group-years in a population of wild savannah baboons. When data were pooled over the entire period, higher-ranking males had greater access to fertile females. However, when we examined successive 6-month blocks, we found variance in the extent to which rank predicted mating success. In some periods, the dominance hierarchy functioned as a queue in which males waited for mating opportunities, so that rank predicted mating success. In other periods, the queuing system broke down, and rank failed to predict mating success when many adult males were in the group, when males in the group differed greatly in age, and when the highest-ranking male maintained his rank for only short periods. The variance within this single population is similar to the variance observed between populations of baboons and between species of primates. Our long-term results provide strong support for the proposition that this variance is not an artefact of methodological differences between short-term studies, but is due to true variance in the extent to which high-ranking males are able to monopolize access to females. © 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.}, Doi = {10.1006/anbe.2003.2106}, Key = {fds304242} } @article{fds227851, Author = {Smith, K and Alberts, SC and Altmann, J}, Title = {Wild female baboons bias their social behaviour towards paternal half-sisters.}, Journal = {Proceedings. Biological sciences}, Volume = {270}, Number = {1514}, Pages = {503-510}, Year = {2003}, Month = {March}, ISSN = {0962-8452}, url = {http://dx.doi.org/10.1098/rspb.2002.2277}, Abstract = {Adult female cercopithecines have long been known to bias their social behaviour towards close maternal kin. However, much less is understood about the behaviour of paternal kin, especially in wild populations. Here, we show that wild adult female baboons bias their affiliative behaviour towards their adult paternal half-sisters in the same manner and to the same extent that they bias their behaviour towards adult maternal half-sisters. Females appear to rely heavily on social familiarity as a means of biasing their behaviour towards paternal half-sisters, but may use phenotype matching as well.}, Doi = {10.1098/rspb.2002.2277}, Key = {fds227851} } @article{fds7899, Author = {Alberts SC and Altmann J}, Title = {Matrix models for primate life history analysis}, Booktitle = {Primate Life Histories and Socioecology}, Publisher = {University of Chicago Press}, Editor = {P. Kappeler and M.E. Pereira}, Year = {2003}, Key = {fds7899} } @article{fds7901, Author = {Altmann J and Alberts SC}, Title = {Intraspecific variability in fertility and offspring survival in a non-human primate: behavioral control of ecological and social sources}, Booktitle = {Offspring: Human Fertility Behavior in Biodemographic Perspective}, Editor = {K. Wachter and R.A. Bulatao}, Year = {2003}, Key = {fds7901} } @article{fds227852, Author = {Alberts, SC and Watts, HE and Altmann, J}, Title = {Queuing and queue jumping: long term patterns of reproductive skew among male savannah baboons}, Journal = {Animal Behaviour}, Volume = {65}, Number = {4}, Pages = {821-840}, Year = {2003}, url = {http://dx.doi.org/10.1006/anbe.2003.2106}, Abstract = {In many animals, variance in male mating success is strongly correlated with male dominance rank or some other measure of fighting ability. Studies in primates, however, have varied greatly in whether they detect a relationship between male dominance rank and mating success. This variability has led to debate about the nature of the relation between rank and mating success in male primates. We contribute to the resolution of this debate by presenting an analysis of the relationship between dominance rank and male mating success over 32 group-years in a population of wild savannah baboons. When data were pooled over the entire period, higher-ranking males had greater access to fertile females. However, when we examined successive 6-month blocks, we found variance in the extent to which rank predicted mating success. In some periods, the dominance hierarchy functioned as a queue in which males waited for mating opportunities, so that rank predicted mating success. In other periods, the queuing system broke down, and rank failed to predict mating success when many adult males were in the group, when males in the group differed greatly in age, and when the highest-ranking male maintained his rank for only short periods. The variance within this single population is similar to the variance observed between populations of baboons and between species of primates. Our long-term results provide strong support for the proposition that this variance is not an artefact of methodological differences between short-term studies, but is due to true variance in the extent to which high-ranking males are able to monopolize access to females. © 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.}, Doi = {10.1006/anbe.2003.2106}, Key = {fds227852} } @article{fds227864, Author = {Storz, JF and Beaumont, MA and Alberts, SC}, Title = {Genetic evidence for long-term population decline in a savannah-dwelling primate: inferences from a hierarchical bayesian model.}, Journal = {Molecular biology and evolution}, Volume = {19}, Number = {11}, Pages = {1981-1990}, Year = {2002}, Month = {November}, url = {http://dx.doi.org/10.1093/oxfordjournals.molbev.a004022}, Abstract = {The purpose of this study was to test for evidence that savannah baboons (Papio cynocephalus) underwent a population expansion in concert with a hypothesized expansion of African human and chimpanzee populations during the late Pleistocene. The rationale is that any type of environmental event sufficient to cause simultaneous population expansions in African humans and chimpanzees would also be expected to affect other codistributed mammals. To test for genetic evidence of population expansion or contraction, we performed a coalescent analysis of multilocus microsatellite data using a hierarchical Bayesian model. Markov chain Monte Carlo (MCMC) simulations were used to estimate the posterior probability density of demographic and genealogical parameters. The model was designed to allow interlocus variation in mutational and demographic parameters, which made it possible to detect aberrant patterns of variation at individual loci that could result from heterogeneity in mutational dynamics or from the effects of selection at linked sites. Results of the MCMC simulations were consistent with zero variance in demographic parameters among loci, but there was evidence for a 10- to 20-fold difference in mutation rate between the most slowly and most rapidly evolving loci. Results of the model provided strong evidence that savannah baboons have undergone a long-term historical decline in population size. The mode of the highest posterior density for the joint distribution of current and ancestral population size indicated a roughly eightfold contraction over the past 1,000 to 250,000 years. These results indicate that savannah baboons apparently did not share a common demographic history with other codistributed primate species.}, Doi = {10.1093/oxfordjournals.molbev.a004022}, Key = {fds227864} } @article{fds304241, Author = {Zinner, D and Alberts, SC and Nunn, CL and Altmann, J}, Title = {Evolutionary biology: significance of primate sexual swellings.}, Journal = {Nature}, Volume = {420}, Number = {6912}, Pages = {142-143}, Year = {2002}, Month = {November}, url = {http://dx.doi.org/10.1038/420142a}, Doi = {10.1038/420142a}, Key = {fds304241} } @article{fds227866, Author = {Altmann, J and Alberts, SC and Altmann, SA and Roy, SB}, Title = {Dramatic change in local climate patterns in the Amboseli basin, Kenya}, Journal = {African Journal of Ecology}, Volume = {40}, Number = {3}, Pages = {248-251}, Publisher = {WILEY}, Year = {2002}, Month = {September}, ISSN = {0141-6707}, url = {http://dx.doi.org/10.1046/j.1365-2028.2002.00366.x}, Abstract = {The Amboseli basin, a semi-arid, open savannah area of southern Kenya, has experienced extensive changes in habitat since the early 1960's. The present report documents patterns of air temperature and rainfall in Amboseli for the 25-year period beginning 1976. Daily temperatures increased dramatically throughout this time period, at a rate almost an order of magnitude greater than that attributed to global warming. Mean daily maximum temperature increased more than did daily minimum (0.275 vs. 0.071°C per annum). Although increases in mean daily maxima were documented for all months of the year, they were greatest during the hottest months, February and March. Annual rainfall varied more than four-fold (x = 346.5 mm, SD = 120.0, range 132.0-553.4 mm), yet did not exhibit any directional or other regular pattern of variability among years over this same 25-year period. Empirical as well as theoretical investigation of relations between such changes in climatic conditions and habitat characteristics are needed at local and regional as well as global scales.}, Doi = {10.1046/j.1365-2028.2002.00366.x}, Key = {fds227866} } @article{fds227772, Author = {Storz, JF and Ramakrishnan, U and Alberts, SC}, Title = {Erratum: Determinants of effective population size for loci with different modes of inheritance (The Journal of Heredity (November-December 2001) 92:6)}, Journal = {Journal of Heredity}, Volume = {93}, Number = {2}, Pages = {155}, Year = {2002}, Month = {July}, Key = {fds227772} } @article{fds227863, Author = {Bronikowski, AM and Alberts, SC and Altmann, J and Packer, C and Carey, KD and Tatar, M}, Title = {The aging baboon: comparative demography in a non-human primate.}, Journal = {Proceedings of the National Academy of Sciences of the United States of America}, Volume = {99}, Number = {14}, Pages = {9591-9595}, Year = {2002}, Month = {July}, ISSN = {0027-8424}, url = {http://dx.doi.org/10.1073/pnas.142675599}, Abstract = {Why do closely related primate genera vary in longevity, and what does this teach us about human aging? Life tables of female baboons (Papio hamadryas) in two wild populations of East Africa and in a large captive population in San Antonio, Texas, provide striking similarities and contrasts to human mortality patterns. For captive baboons at the Southwest Foundation for Biomedical Research, we estimate the doubling time of adult mortality rate as 4.8 years. Wild females in free-living populations in Tanzania and in Kenya showed doubling times of 3.5 and 3.8 years, respectively. Although these values are considerably faster than the estimates of 7-8 years for humans, these primates share a demographic feature of human aging: within each taxon populations primarily vary in the level of Gompertz mortality intercept (frailty) and vary little in the demographic rate of aging. Environmental and genetic factors within taxa appear to affect the level of frailty underlying senescence. In contrast, primate taxa are differentiated by rates of demographic aging, even if they cannot be characterized by species-specific lifespan.}, Doi = {10.1073/pnas.142675599}, Key = {fds227863} } @article{fds227773, Author = {Storz, JF and Ramakrishnan, U and Alberts, SC}, Title = {Erratum: Determinants of effective population size for loci with different modes of inheritance (Journal of Heredity (November/December 2001) 92:6)}, Journal = {Journal of Heredity}, Volume = {93}, Number = {3}, Pages = {230}, Year = {2002}, Month = {May}, Key = {fds227773} } @article{fds227877, Author = {Storz, JF and Ramakrishnan, U and Alberts, SC}, Title = {Genetic effective size of a wild primate population: influence of current and historical demography.}, Journal = {Evolution; international journal of organic evolution}, Volume = {56}, Number = {4}, Pages = {817-829}, Year = {2002}, Month = {April}, ISSN = {0014-3820}, url = {http://dx.doi.org/10.1111/j.0014-3820.2002.tb01392.x}, Abstract = {A comprehensive assessment of the determinants of effective population size (N(e)) requires estimates of variance in lifetime reproductive success and past changes in census numbers. For natural populations, such information can be best obtained by combining longitudinal data on individual life histories and genetic marker-based inferences of demographic history. Independent estimates of the variance effective size (N(ev), obtained from life-history data) and the inbreeding effective size (N((eI), obtained from genetic data) provide a means of disentangling the effects of current and historical demography. The purpose of this study was to assess the demographic determinants of N(e) in one of the most intensively studied natural populations of a vertebrate species: the population of savannah baboons (Papio cynocephalus) in the Amboseli Basin, southern Kenya. We tested the hypotheses that N(eV) < N < N(eI) (where N = population census number) due to a recent demographic bottleneck. N(eV) was estimated using a stochastic demographic model based on detailed life-history data spanning a 28-year period. Using empirical estimates of age-specific rates of survival and fertility for both sexes, individual-based simulations were used to estimate the variance in lifetime reproductive success. The resultant values translated into an N(eV)/N estimate of 0.329 (SD = 0.116, 95% CI = 0.172-0.537). Historical N(eI), was estimated from 14-locus microsatellite genotypes using a coalescent-based simulation model. Estimates of N(eI) were 2.2 to 7.2 times higher than the contemporary census number of the Amboseli baboon population. In addition to the effects of immigration, the disparity between historical N(eI) and contemporary N is likely attributable to the time lag between the recent drop in census numbers and the rate of increase in the average probability of allelic identity-by-descent. Thus, observed levels of genetic diversity may primarily reflect the population's prebottleneck history rather than its current demography.}, Doi = {10.1111/j.0014-3820.2002.tb01392.x}, Key = {fds227877} } @article{fds304240, Author = {Semple, S and McComb, K and Alberts, S and Altmann, J}, Title = {Information content of female copulation calls in yellow baboons.}, Journal = {American journal of primatology}, Volume = {56}, Number = {1}, Pages = {43-56}, Year = {2002}, Month = {January}, ISSN = {0275-2565}, url = {http://dx.doi.org/10.1002/ajp.1062}, Abstract = {In a wide variety of animal species, females produce vocalizations just before, during, or immediately after copulation. Observational and experimental evidence indicates that these copulation calls are sexually selected traits, functioning to promote competition between males for access to the calling female. In this paper, we present an acoustic analysis of variation in the form of copulation calls of female yellow baboons, Papio cynocephalus cynocephalus. In particular, we examine whether information about three factors-the calling female's reproductive state, the occurrence or absence of ejaculation, and the dominance rank of the mating male-is encoded in call structure and hence is potentially available to male receivers attending to the signal. Although several features of copulation calls were correlated with each of these factors, when all three were included in multiple regressions only reproductive state and rank of the mating male had independent effects on call form. These findings indicate that female copulation calls in this species signal information about the proximity to ovulation of the calling female and also the relative competitive strength of her mating partner.}, Doi = {10.1002/ajp.1062}, Key = {fds304240} } @article{fds227878, Author = {Semple, S and McComb, K and Alberts, SC and Altmann, J}, Title = {Sources of variation in the copulation calls of female yellow baboons}, Journal = {American Journal of Primatology}, Volume = {56}, Number = {1}, Pages = {43-56}, Year = {2002}, ISSN = {0275-2565}, url = {http://dx.doi.org/10.1002/ajp.1062}, Abstract = {In a wide variety of animal species, females produce vocalizations just before, during, or immediately after copulation. Observational and experimental evidence indicates that these copulation calls are sexually selected traits, functioning to promote competition between males for access to the calling female. In this paper, we present an acoustic analysis of variation in the form of copulation calls of female yellow baboons, Papio cynocephalus cynocephalus. In particular, we examine whether information about three factors - The calling female's reproductive state, the occurrence or absence of ejaculation, and the dominance rank of the mating male - Is encoded in call structure and hence is potentially available to male receivers attending to the signal. Although several features of copulation calls were correlated with each of these factors, when all three were included in multiple regressions only reproductive state and rank of the mating male had independent effects on call form. These findings indicate that female copulation calls in this species signal information about the proximity to ovulation of the calling female and also the relative competitive strength of her mating partner. Am. J. Primatol. 56:43-56, 2002. © 2002 Wiley-Liss, Inc.}, Doi = {10.1002/ajp.1062}, Key = {fds227878} } @article{fds227881, Author = {Zinner, D and Albert, SC and Nunn, CL and Altmann, J}, Title = {Significance of primate sexual swellings}, Journal = {Nature}, Volume = {420}, Number = {6912}, Pages = {142-143}, Year = {2002}, url = {http://dx.doi.org/10.1038/420142a}, Doi = {10.1038/420142a}, Key = {fds227881} } @article{fds227865, Author = {Storz, JF and Ramakrishnan, U and Alberts, SC}, Title = {Determinants of effective population size for loci with different modes of inheritance.}, Journal = {The Journal of heredity}, Volume = {92}, Number = {6}, Pages = {497-502}, Year = {2001}, Month = {November}, ISSN = {0022-1503}, url = {http://dx.doi.org/10.1093/jhered/92.6.497}, Abstract = {Here we report an assessment of the determinants of effective population size (N(e)) in species with overlapping generations. Specifically, we used a stochastic demographic model to investigate the influence of different life-history variables on N(e)/N (where N = population census number) and the influence of sex differences in life-history variables on N(e) for loci with different modes of inheritance. We applied an individual-based modeling approach to two datasets: one from a natural population of savannah baboons (Papio cynocephalus) in the Amboseli basin of southern Kenya and one from a human tribal population (the Gainj of Papua New Guinea). Simulation-based estimates of N(e)/N averaged 0.329 for the Amboseli baboon population (SD = 0.116, 95% CI = 0.172 - 0.537) and 0.786 for the Gainj (SD = 0.184, 95% CI = 0.498 - 1.115). Although variance in male fitness had a substantial impact on N(e)/N in each of the two primate populations, ratios of N(e) values for autosomal and sex-linked loci exhibited no significant departures from Poisson-expected values. In each case, similarities in sex-specific N(e) values were attributable to the unexpectedly high variance in female fitness. Variance in male fitness resulted primarily from age-dependent variance in reproductive success, whereas variance in female fitness resulted primarily from stochastic variance in survival during the reproductive phase.}, Doi = {10.1093/jhered/92.6.497}, Key = {fds227865} } @article{fds227855, Author = {Alberts, SC and Altmann, J}, Title = {Immigration and hybridization patterns of yellow and anubis baboons in and around Amboseli, Kenya.}, Journal = {American journal of primatology}, Volume = {53}, Number = {4}, Pages = {139-154}, Year = {2001}, Month = {April}, ISSN = {0275-2565}, url = {http://www.ncbi.nlm.nih.gov/pubmed/11283975}, Abstract = {In 1986, Samuels and Altmann reported evidence for a hybrid zone between Papio anubis and Papio cynocephalus in Amboseli, Kenya, in a baboon population that has been the subject of long-term study since 1971 [Samuels & Altmann, International Journal of Primatology 7:131-138, 1986]. In the current report we document ongoing patterns of hybridization in Amboseli between anubis and yellow baboons. In July 2000, we exhaustively scored living members of study groups for their degree of hybridity, using seven phenotypic characteristics (five in juveniles). We also scored all former members of study groups on the basis of photographic records, field notes, and observer recollections. A total of five anubis males and 11 males with hybrid phenotypes have immigrated into study groups over the course of the long-term study, and immigrations by hybrid males have increased in frequency over time. Further, the increasing frequency of hybrid phenotypes among animals born into study groups indicates that anubis and hybrid males have successfully reproduced in study groups. However, hybrid phenotypes and anubis immigrations were limited to groups in the southwestern portion of the Amboseli basin, with no hybrids occurring in the six eastern groups. Finally, we present evidence that anubis and hybrid males in Amboseli exhibit patterns of natal dispersal that are different from those of yellow males in Amboseli: males with anubis or hybrid phenotypes were significantly more likely to immigrate as juveniles or young subadults than were yellow males.}, Doi = {10.1002/ajp.1}, Key = {fds227855} } @article{fds7909, Author = {Alberts SC and Altmann J}, Title = {Immigration and hybridization patterns of yellow and anubis baboons in Amboseli, Kenya}, Journal = {American Journal of Primatology}, Volume = {53}, Pages = {139-154}, Year = {2001}, Key = {fds7909} } @article{fds227849, Author = {Storz, JF and Ramakrishnan, U and Alberts, SC}, Title = {Determinants of effective population size for loci with different modes of inheritance}, Journal = {Journal of Heredity}, Volume = {92}, Pages = {197-502}, Year = {2001}, Key = {fds227849} } @article{fds227879, Author = {Smith, KL and Alberts, SC and Bayes, MK and Bruford, MW and Altmann, J and Ober, C}, Title = {Cross-species amplification, non-invasive genotyping, and non-Mendelian inheritance of human STRPs in Savannah baboons.}, Journal = {American journal of primatology}, Volume = {51}, Number = {4}, Pages = {219-227}, Year = {2000}, Month = {August}, url = {http://dx.doi.org/10.1002/1098-2345(200008)51:4<219::aid-ajp1>3.0.co;2-g}, Abstract = {Twenty-nine human microsatellite primer pairs were screened for their utility in the cross-species amplification of baboon DNA derived from both blood and feces as part of a larger study to identify paternal half sisters in a population of wild baboons (Papio cynocephalus). Forty-one percent (12/29) of the human primers successfully amplified baboon DNA. Of these 12 primers, six amplified fragments that were both polymorphic and heterozygous (mean number of alleles = 6, mean heterozygosity = 87%) and yielded repeatable results. However, only five of these six simple tandem repeat polymorphisms (STRPs) showed patterns of Mendelian inheritance (i.e., mothers and offspring shared at least one allele at each locus), and were therefore useful for determining relatedness between individuals. Analysis of the sixth primer revealed non-Mendelian inheritance, i.e., three of the six known mother-daughter pairs had no shared alleles. This failure was probably due to non-specific fragment amplification, and may have resulted from a different STRP locus being amplified in mother and daughter. This finding highlights the importance of sampling DNA from known parent-offspring pairs when screening microsatellite primers for genetic studies. Multiple, independent replications of genotypes and Mendelian checks are both particularly important when using cross-species amplification or when using a low-quality source of DNA.}, Doi = {10.1002/1098-2345(200008)51:4<219::aid-ajp1>3.0.co;2-g}, Key = {fds227879} } @article{fds304239, Author = {Bayes, MK and Smith, KL and Alberts, SC and Altmann, J and Bruford, MW}, Title = {Testing the reliability of microsatellite typing from faecal DNA in the savannah baboon}, Journal = {Conservation Genetics}, Volume = {1}, Number = {2}, Pages = {173-176}, Year = {2000}, Month = {January}, url = {http://dx.doi.org/10.1023/A:1026595324974}, Doi = {10.1023/A:1026595324974}, Key = {fds304239} } @article{fds227880, Author = {Bayes, MK and Smith, KL and Alberts, SC and Cheesman, DJ and Altmann, J and Bruford, MW}, Title = {Fecal DNA genotyping in the savannah baboons: history, problems and data}, Journal = {Conservation Genetics}, Volume = {1}, Number = {2}, Pages = {173-176}, Year = {2000}, Key = {fds227880} } @article{fds227875, Author = {Alberts, SC}, Title = {Thirteen Mhc-DQA1 alleles from two populations of baboons.}, Journal = {Immunogenetics}, Volume = {49}, Number = {9}, Pages = {825-827}, Year = {1999}, Month = {August}, ISSN = {0093-7711}, url = {http://www.ncbi.nlm.nih.gov/pubmed/10398813}, Doi = {10.1007/s002510050560}, Key = {fds227875} } @article{fds227876, Author = {Alberts, SC}, Title = {Paternal kin discrimination in wild baboons.}, Journal = {Proceedings. Biological sciences}, Volume = {266}, Number = {1427}, Pages = {1501-1506}, Year = {1999}, Month = {July}, ISSN = {0962-8452}, url = {http://www.ncbi.nlm.nih.gov/pubmed/10457619}, Abstract = {Mammals commonly avoid mating with maternal kin, probably as a result of selection for inbreeding avoidance. Mating with paternal kin should be selected against for the same reason. However, identifying paternal kin may be more difficult than identifying maternal kin in species where the mother mates with more than one male. Selection should nonetheless favour a mechanism of paternal kin recognition that allows the same level of discrimination among paternal as among maternal kin, but the hypothesis that paternal kin avoid each other as mates is largely untested in large mammals such as primates. Here I report that among wild baboons, Papio cynocephalus, paternal siblings exhibited lower levels of affiliative and sexual behaviour during sexual consortships than non-kin, although paternal siblings were not significantly less likely to consort than non-kin. I also examined age proximity as a possible social cue of paternal relatedness, because age cohorts are likely to be paternal sibships. Pairs born within two years of each other were less likely to engage in sexual consortships than pairs born at greater intervals, and were less affiliative and sexual when they did consort. Age proximity may thus be an important social cue for paternal relatedness, and phenotype matching based on shared paternal traits may play a role as well.}, Doi = {10.1098/rspb.1999.0807}, Key = {fds227876} } @article{fds227874, Author = {Sapolsky, RM and Alberts, SC and Altmann, J}, Title = {Hypercortisolism associated with social subordinance or social isolation among wild baboons.}, Journal = {Archives of general psychiatry}, Volume = {54}, Number = {12}, Pages = {1137-1143}, Year = {1997}, Month = {December}, ISSN = {0003-990X}, url = {http://dx.doi.org/10.1001/archpsyc.1997.01830240097014}, Abstract = {<h4>Background</h4>The phenomena of basal hypercortisolism and of dexamethasone resistance have long intrigued biological psychiatrists, and much is still unknown as to the causes and consequences of such adrenocortical hyperactivity in various neuropsychiatric disorders. We have analyzed basal cortisol concentrations and adrenocortical responsiveness to dexamethasone in a population of wild baboons living in a national park in Kenya. We tested whether social subordinance in a primate is associated with dexamethasone resistance. Furthermore, we examined whether individual differences in adrenocortical measurements were predicted by the extent of social affiliation in these animals.<h4>Methods</h4>Seventy yellow baboons (Papio cynocephalus) were anesthetized and injected with 5 mg of dexamethasone; the cortisol response was monitored for 6 hours. The animals were of both sexes in a range of ages and had known ranks in the dominance hierarchies within their troops. Extensive behavioral data were available for a subset of 12 adult males who were anesthetized under circumstances that also allowed for the determination of basal cortisol concentrations.<h4>Results</h4>The socially subordinate baboons were less responsive to dexamethasone than were the dominant ones; as one manifestation of this, postdexamethasone cortisol values were more than 3 times higher in the dozen lowest-ranking animals compared with the dozen highest. In addition, socially isolated males had elevated basal cortisol concentrations and showed a trend toward relative dexamethasone resistance.<h4>Conclusions</h4>Our findings indicate that social status and degree of social affilitation can influence adrenocortical profiles; specifically, social subordinance or social isolation were associated in our study with hypercortisolism or feedback resistance.}, Doi = {10.1001/archpsyc.1997.01830240097014}, Key = {fds227874} } @article{fds227873, Author = {Altmann, J and Alberts, SC and Haines, SA and Dubach, J and Muruthi, P and Coote, T and Geffen, E and Cheesman, DJ and Mututua, RS and Saiyalel, SN and Wayne, RK and Lacy, RC and Bruford, MW}, Title = {Behavior predicts genes structure in a wild primate group.}, Journal = {Proceedings of the National Academy of Sciences of the United States of America}, Volume = {93}, Number = {12}, Pages = {5797-5801}, Year = {1996}, Month = {June}, ISSN = {0027-8424}, url = {http://dx.doi.org/10.1073/pnas.93.12.5797}, Abstract = {The predictability of genetic structure from social structure and differential mating success was tested in wild baboons. Baboon populations are subdivided into cohesive social groups that include multiple adults of both sexes. As in many mammals, males are the dispersing sex. Social structure and behavior successfully predicted molecular genetic measures of relatedness and variance in reproductive success. In the first quantitative test of the priority-of-access model among wild primates, the reproductive priority of dominant males was confirmed by molecular genetic analysis. However, the resultant high short-term variance in reproductive success did not translate into equally high long-term variance because male dominance status was unstable. An important consequence of high but unstable short-term variance is that age cohorts will tend to be paternal sibships and social groups will be genetically substructured by age.}, Doi = {10.1073/pnas.93.12.5797}, Key = {fds227873} } @article{fds227872, Author = {Alberts, SC and Altmann, J and Wilson, ML}, Title = {Mate guarding constrains foraging activity of male baboons}, Journal = {Animal Behaviour}, Volume = {51}, Number = {6}, Pages = {1269-1277}, Publisher = {Elsevier BV}, Year = {1996}, Month = {January}, url = {http://dx.doi.org/10.1006/anbe.1996.0131}, Abstract = {For many species, mate guarding results in dramatic departures from normal behaviour that reflect compromised attention to feeding and other activities. Such departures have previously been difficult to document in primates, however. Data were gathered on two aspects of male behaviour that were predicted to be constrained during consortships, individual travel distance and duration of feeding bouts, for wild male baboons, Papio cynocephalus, in and out of mate-guarding episodes. In each case, consorting males were compared with themselves outside of consortships, and, in the case of distance travelled, they were compared also with non- consorting males matched for sample time and location. Males travelled significantly shorter distances while consorting than while not consorting, with the result that consorting males travelled distances similar to those travelled by females. Males also had significantly shorter feeding bouts while consorting. The shorter travel distances and feeding bouts experienced by consorting males may represent important constraints on male foraging activity, and probably result in decreased energy intake during mate guarding. Seasonal and non-seasonal breeding patterns will have different consequences for the magnitude of fluctuations in energy stores and depletions experienced during mate guarding, and costs of mate guarding in species that breed non-seasonally will be more difficult to document because they are necessarily smaller and temporally dispersed. When considered across the lifespan, however, mate guarding costs to non-seasonal breeders may equal or exceed costs to seasonal breeders.}, Doi = {10.1006/anbe.1996.0131}, Key = {fds227872} } @article{fds227871, Author = {Alberts, SC and Altmann, J}, Title = {Preparation and activation: determinants of age at reproductive maturity in male baboons}, Journal = {Behavioral Ecology and Sociobiology}, Volume = {36}, Number = {6}, Pages = {397-406}, Publisher = {Springer Nature}, Year = {1995}, Month = {June}, ISSN = {0340-5443}, url = {http://dx.doi.org/10.1007/BF00177335}, Abstract = {Age at maturity is a particularly important life history trait, but maturational data are rare for males in natural populations of mammals. Here we provide information on three maturational milestones and their social and demographic correlates among 43 wild male baboons, Papio cynocephalus, in a natural population in Amboseli National Park, Kenya. We examined (1) age at testicular enlargement, which signals puberty and the onset of subadulthood, (2) age at attainment of adult dominance rank, which we consider to be the beginning of adulthood, and (3) age at first sexual consortship, which is the best measure available for age at first reproduction in male baboons. Testicular enlargement (median age = 5.69 years) occurred earlier among sons of high ranking mothers, and was not influenced by rainfall or seasonality. Attainment of adult dominance rank (median age = 7.41 years) was also accelerated among sons of high-ranking mothers, and among males whose mothers had died while the males were juveniles. First sexual consortship (median age = 7.92 years) was not influenced directly by maternal characteristics, but attainment of adult dominance rank always preceded first consortship. The lag time between attainment of adult rank and first consortship (median = 2.5 months; range = 5-526 days), was predicted by the number of sexually cycling females in the group when the male attained rank, and by how high ranking the male became in his first months as an adult. We suggest that the age at which a male baboon is ready to begin reproducing is influenced by a relatively stable maternal characteristic that exerts its influence early in development, but the timing with which this potential is realized depends on activation by more proximate, often stochastic triggers such as female availability. This two-level organization of influences is likely to contribute to the variance both in age at first reproduction and in lifetime fitness. Differences in the relative magnitude of the two levels will lead to both intra- and interspecific variability in the opportunity for maternal selection and sexual selection. © 1995 Springer-Verlag.}, Doi = {10.1007/BF00177335}, Key = {fds227871} } @article{fds227870, Author = {Alberts, SC and Altmann, J}, Title = {Balancing costs and opportunities: Dispersal in male baboons}, Journal = {American Naturalist}, Volume = {145}, Number = {2}, Pages = {279-306}, Publisher = {University of Chicago Press}, Year = {1995}, Month = {January}, url = {http://dx.doi.org/10.1086/285740}, Doi = {10.1086/285740}, Key = {fds227870} } @article{fds227869, Author = {Alberts, SC}, Title = {Vigilance in young baboons: Effects of habitat, age, sex and maternal rank on glance rate}, Journal = {Animal Behaviour}, Volume = {47}, Number = {4}, Pages = {749-755}, Publisher = {Elsevier BV}, Year = {1994}, Month = {January}, url = {http://dx.doi.org/10.1006/anbe.1994.1107}, Abstract = {Glance rates, a measure of vigilance, were sampled in infant and young juvenile yellow baboons, Papio cynocephalus, in Amboseli, Kenya, to test ecological and social predictions about the ontogeny of vigilance. Glance rates of young baboons did not vary between closed and open habitats, but did vary with sex, maternal rank and age. Daughters of low-ranking mothers glanced significantly more often than daughters of high-ranking mothers, and the converse was true for males. Glance rates of females, but not males, decreased significantly between 6 and 24 months of age. © 1994 The Association for the Study of Animal Behaviour.}, Doi = {10.1006/anbe.1994.1107}, Key = {fds227869} } @article{fds227862, Author = {Alberts, SC and Ober, C}, Title = {Genetic variability in the major histocompatibility complex: A review of non‐pathogen‐mediated selective mechanisms}, Journal = {American Journal of Physical Anthropology}, Volume = {36}, Number = {17 S}, Pages = {71-89}, Publisher = {WILEY}, Year = {1993}, Month = {January}, url = {http://dx.doi.org/10.1002/ajpa.1330360606}, Abstract = {The extraordinary genetic polymorphism observed in the major histocompatibility complex (MHC) of the vertebrate genome has attracted the attention of researchers for decades. In almost all taxa that have been investigated, levels of polymorphism are remarkably high. Several mechanisms have been proposed to explain the maintenance of genetic diversity at the MHC, including pathogen‐driven natural selection, selection driven by maternal‐fetal interactions, and negative assortative mating. In this review we discuss the evidence for the latter two mechanisms in human and animal populations. We begin with a description of the structure and function of the MHC, particularly in humans. Then, evidence for natural selection acting on MHC genes, in the form of homozygote deficiencies observed in human population isolates, is discussed. The two major candidates for mechanisms of non‐pathogen‐driven selection, maternal‐fetal interactions and MHC‐based mate choice, are described in detail and their implications are discussed. © 1993 Wiley‐Liss, Inc. Copyright © 1993 Wiley‐Liss, Inc., A Wiley Company}, Doi = {10.1002/ajpa.1330360606}, Key = {fds227862} } @article{fds227861, Author = {Alberts, SC and Sapolsky, RM and Altmann, J}, Title = {Behavioral, endocrine, and immunological correlates of immigration by an aggressive male into a natural primate group.}, Journal = {Hormones and behavior}, Volume = {26}, Number = {2}, Pages = {167-178}, Year = {1992}, Month = {June}, ISSN = {0018-506X}, url = {http://dx.doi.org/10.1016/0018-506x(92)90040-3}, Abstract = {A very aggressive young adult male entered one of three long-term study groups of yellow baboons. Papio cynocephalus, approximately 3 weeks after an immobilization project began. The immigrant male's rate of agonistic encounters was appreciably higher than average, and these interactions disproportionately involved adult females as targets. Basal cortisol concentrations were higher and total lymphocyte counts lower for individuals immobilized during the immigration situation than for other individuals; these effects were greater for females than for males. Among animals whose endocrine data were obtained during the immigration period, some were specific targets of the immigrant male's aggression and others were not. Lymphocyte counts were significantly lower for those individuals who were victims of the male's aggression than for noninvolved individuals; a nonsignificant tendency toward higher basal cortisol concentrations for victims was observed as well. The immigrant male himself had a high basal cortisol concentration, a low lymphocyte count, and a testosterone concentration that was triple the average for adult males and almost double the second highest value in the population.}, Doi = {10.1016/0018-506x(92)90040-3}, Key = {fds227861} } @article{fds227860, Author = {Altmann, J and Alberts, SC and Sapolsky, RM}, Title = {Endocrine and developmental correlates of unilateral cryptorchidism in a wild baboons}, Journal = {American Journal of Primatology}, Volume = {26}, Number = {4}, Pages = {309-314}, Publisher = {WILEY}, Year = {1992}, url = {http://dx.doi.org/10.1002/ajp.1350260407}, Abstract = {A wild, group‐living 8.5‐year‐old adult baboon was found to have only a single palpable testicle, the only case of cryptorchidism found among more than 200 males that we have examined. This young adult had an unusually small body size for his age, one that was comparable to that of immature males two years younger, and during maturation his body mass was increasingly small for his age. As a young adult, he also had very low testosterone concentrations, which, in combination with his small size, history of impaired growth, and the absence of any obvious scars around the scrotum, suggest that this is a case of spontaneous unilateral cryptorchidism of unknown cause rather than one of monorchidism arising from injury. Despite striking differences in his growth, adult body size, and testosterone levels, the male's cryptorchidism seemed to have relatively little effect on his social and sexual maturation in his natal group. Nonetheless, it may be related to his inability to gain entry into another group after dispersal. Copyright © 1992 Wiley‐Liss, Inc., A Wiley Company}, Doi = {10.1002/ajp.1350260407}, Key = {fds227860} } @article{fds227868, Author = {Altmann, J and Alberts, S}, Title = {Body mass and growth rates in a wild primate population}, Journal = {Oecologia}, Volume = {72}, Number = {1}, Pages = {15-20}, Publisher = {Springer Nature}, Year = {1987}, Month = {April}, ISSN = {0029-8549}, url = {http://dx.doi.org/10.1007/BF00385038}, Abstract = {We obtined data on body mass and growth rates for the immature members of two groups of wild baboons in Amboseli National Park, Kenya. Data were collected without feeding, trapping, or handling. The data were separated into cross-sectional and longitudinal components, allowing both the examination of body mass-age relationships and the calculation of growth rates for individuals. For animals less than three years old, body mass was wellperedicted from age by a linear model. Differences based on social group membership were small but consistent, and their origins are discussed. We detected no differences in body mass based on sex or on maternal dominance rank. For older juveniles, those three to seven years of age, a better fit was obtained from log of mass than by mass in a linear model. This was also true for the cross-sectional data set over the whole age range (zero to seven years). For older juveniles, samples were too small for quantitative analysis of differences based on sex, rank, or group membership, but trends in the data are indicated. Growth rates derived from repeat measures of body mass for 38 animals are presented and discussed. The growth rate values obtained in this study are consistent with data from cross-sectional studies of other wild baboon populations; these values for wild baboons are consistently one-half to one-third lower than growth rate values for well-provisioned captive baboons and equivalent to captive baboons fed a low-protein diet. Comparisons between primates and other mammals in the primate size range raise questions concerning ecological and behavioral constraints on primate growth rates; some possible mechanisms of constraint are suggested. © 1987 Springer-Verlag.}, Doi = {10.1007/BF00385038}, Key = {fds227868} } @article{fds227859, Author = {Alberts, SC}, Title = {Parental care in captive siamangs (Hylobates syndactylus)}, Journal = {Zoo Biology}, Volume = {6}, Number = {4}, Pages = {401-406}, Publisher = {WILEY}, Year = {1987}, url = {http://dx.doi.org/10.1002/zoo.1430060414}, Abstract = {Siamangs exhibit paternal care to the extent that the male of a monogamous unit carries its infant offspring beginning late in the infant's first year of life. Field studies have documented this but without behavioral detail. It has been hypothesized that the transfer is facilitated by a desertion of the infant by the female. An infant siamang born in captivity at the Washington Park Zoo, Portland, Oregon, was observed through its first year of life. The infant transfer to the male was documented in captivity and was associated with a high rate of infant‐initiated contact with the male and a high rate of infant retrieval by the female. The study concludes that the infant probably played a key role in facilitating the transfer to the male. Copyright © 1987 Wiley‐Liss, Inc., A Wiley Company}, Doi = {10.1002/zoo.1430060414}, Key = {fds227859} } %% Papers Submitted @article{fds219921, Author = {P.I. Chiyo and J.W. Wilson and C.M. Moss and S.C. Alberts}, Title = {The influence of ecology and reproductive opportunities on group size in male African elephants}, Journal = {Behavioral Ecology and Sociobiology}, Year = {2013}, Key = {fds219921} } @article{fds219894, Author = {E.A. Archie and J. Altmann and S.C. Alberts}, Title = {Injury and immune costs of reproduction in a long-lived female primate}, Journal = {Behavioral Ecology}, Year = {2013}, Key = {fds219894} } @article{fds219896, Author = {A.J. Lea and N. Learn and M.J. Theus and J. Altmann and S.C. Alberts}, Title = {Dynamic patterns of dominance rank attainment in female baboons (Papio cynocephalus)}, Journal = {Animal Behaviour}, Year = {2013}, Key = {fds219896} } %% Book Chapters @misc{fds183131, Author = {S.C. Alberts}, Title = {Magnitude and sources of variation in male reproductive performance}, Pages = {412-431}, Booktitle = {The Evolution of Primate Societies}, Publisher = {University of Chicago Press}, Address = {Chicago}, Editor = {J. Mitani and J. Call and P. Kappeler and R. Palombit and J.B. Silk}, Year = {2012}, Key = {fds183131} } @misc{fds198069, Author = {Alberts SC and Altmann J}, Title = {The Amboseli Baboon Research Project: Themes of continuity and change}, Pages = {261-288}, Booktitle = {Long-term field studies of primates}, Publisher = {Springer Verlag}, Editor = {P Kappeler and DP Watts}, Year = {2012}, Key = {fds198069} } @misc{fds166356, Author = {Archie EA and Fitzpatrick CL and Moss CJ and Alberts SC}, Title = {The population genetics of the Amboseli and Kilimanjaro elephants}, Pages = {37-47}, Booktitle = {Amboseli Elephants: A Long-term Perspective on a Long-lived Mammal}, Publisher = {University of Chicago Press}, Editor = {C. Moss and H. Croze and P. Lee}, Year = {2011}, Key = {fds166356} } @misc{fds166357, Author = {Archie EA and Moss CJ and Alberts SC}, Title = {Friends and relations: kinship and the nature of female elephant social relationships}, Pages = {238-245}, Booktitle = {Amboseli Elephants: A Long-term Perspective on a Long-lived Mammal}, Publisher = {University of Chicago Press}, Editor = {C. Moss and H. Croze and P. Lee}, Year = {2011}, Key = {fds166357} } @misc{fds166358, Author = {J.A. Hollister-Smith and J.H. Poole and C.J. Moss and S.C. Alberts}, Title = {Genetic paternity analysis of the Amboseli elephant population}, Pages = {274-275}, Booktitle = {Amboseli Elephants: A Long-term Perspective on a Long-lived Mammal}, Publisher = {University of Chicago Press}, Editor = {C. Moss and H. Croze and P. Lee}, Year = {2011}, Key = {fds166358} } @misc{fds140246, Author = {Loisel DA and Alberts SC and Ober C}, Title = {Functional significance of MHC variation in mate choice, reproductive outcome, and disease risk}, Series = {2nd edition}, Pages = {95-108}, Booktitle = {Evolution in Health and Disease}, Publisher = {Oxford University Press}, Address = {Oxford, UK}, Editor = {SC Stearns and J Koella}, Year = {2008}, Key = {fds140246} } @misc{fds366833, Author = {Alberts, SC and Altmann, J}, Title = {The Evolutionary Past and the Research Future: Environmental Variation and Life History Flexibility in a Primate Lineage}, Pages = {277-303}, Booktitle = {REPRODUCTION AND FITNESS IN BABOONS}, Publisher = {Kluwer Academic Publishers}, Editor = {L. Swedell and S. Leigh}, Year = {2006}, ISBN = {978-0-387-30688-9}, Key = {fds366833} } @misc{fds366834, Author = {Alberts, SC and Hollister-Smith, JA and Mututua, RS and Sayialel, SN and Muruthi, PM and Warutere, JK and Altmann, J}, Title = {Seasonality and long-term change in a savanna environment}, Pages = {157-196}, Booktitle = {Seasonality in Primates}, Publisher = {Cambridge University Press}, Editor = {D. K. Brockman and C. P. van Schaik}, Year = {2005}, Month = {November}, url = {http://dx.doi.org/10.1017/cbo9780511542343.007}, Doi = {10.1017/cbo9780511542343.007}, Key = {fds366834} } %% Book Reviews @article{fds183138, Author = {S.C. Alberts}, Title = {Review of "Sexual Coercion in Primates and Humans: An Evolutionary Perspective on Male Aggression Against Females", edited by MN Muller and RW Wrangham, Cambridge University Press. 2009.}, Journal = {Quarterly Review of Biology}, Volume = {84}, Pages = {413-414}, Year = {2010}, Key = {fds183138} } %% Other @misc{fds183133, Author = {S.C. Alberts}, Title = {Dispatch: Primatology: "A Faithful Friend is the Medicine of Life"}, Journal = {Current Biology}, Volume = {20}, Pages = {1359-1361}, Year = {2010}, Key = {fds183133} } | ||
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