%% Papers Published
@article{fds374278,
Author = {Bornbusch, SL and Power, ML and Schulkin, J and Drea, CM and Maslanka,
MT and Muletz-Wolz, CR},
Title = {Integrating microbiome science and evolutionary medicine
into animal health and conservation.},
Journal = {Biological reviews of the Cambridge Philosophical
Society},
Volume = {99},
Number = {2},
Pages = {458-477},
Year = {2024},
Month = {April},
url = {http://dx.doi.org/10.1111/brv.13030},
Abstract = {Microbiome science has provided groundbreaking insights into
human and animal health. Similarly, evolutionary medicine -
the incorporation of eco-evolutionary concepts into
primarily human medical theory and practice - is
increasingly recognised for its novel perspectives on modern
diseases. Studies of host-microbe relationships have been
expanded beyond humans to include a wide range of animal
taxa, adding new facets to our understanding of animal
ecology, evolution, behaviour, and health. In this review,
we propose that a broader application of evolutionary
medicine, combined with microbiome science, can provide
valuable and innovative perspectives on animal care and
conservation. First, we draw on classic ecological
principles, such as alternative stable states, to propose an
eco-evolutionary framework for understanding variation in
animal microbiomes and their role in animal health and
wellbeing. With a focus on mammalian gut microbiomes, we
apply this framework to populations of animals under human
care, with particular relevance to the many animal species
that suffer diseases linked to gut microbial dysfunction
(e.g. gut distress and infection, autoimmune disorders,
obesity). We discuss diet and microbial landscapes (i.e. the
microbes in the animal's external environment), as two
factors that are (i) proposed to represent evolutionary
mismatches for captive animals, (ii) linked to gut
microbiome structure and function, and (iii) potentially
best understood from an evolutionary medicine perspective.
Keeping within our evolutionary framework, we highlight the
potential benefits - and pitfalls - of modern microbial
therapies, such as pre- and probiotics, faecal microbiota
transplants, and microbial rewilding. We discuss the
limited, yet growing, empirical evidence for the use of
microbial therapies to modulate animal gut microbiomes
beneficially. Interspersed throughout, we propose 12
actionable steps, grounded in evolutionary medicine, that
can be applied to practical animal care and management. We
encourage that these actionable steps be paired with
integration of eco-evolutionary perspectives into our
definitions of appropriate animal care standards. The
evolutionary perspectives proposed herein may be best
appreciated when applied to the broad diversity of species
under human care, rather than when solely focused on humans.
We urge animal care professionals, veterinarians,
nutritionists, scientists, and others to collaborate on
these efforts, allowing for simultaneous care of animal
patients and the generation of valuable empirical
data.},
Doi = {10.1111/brv.13030},
Key = {fds374278}
}
@article{fds369332,
Author = {Grebe, NM and Sheikh, A and Ohannessian, L and Drea,
CM},
Title = {Effects of oxytocin receptor blockade on dyadic social
behavior in monogamous and non-monogamous
Eulemur.},
Journal = {Psychoneuroendocrinology},
Volume = {150},
Pages = {106044},
Year = {2023},
Month = {April},
url = {http://dx.doi.org/10.1016/j.psyneuen.2023.106044},
Abstract = {A prominent body of research spanning disciplines has been
focused on the potential underlying role for oxytocin in the
social signatures of monogamous mating bonds. Behavioral
differences between monogamous and non-monogamous vole
species, putatively mediated by oxytocinergic function,
constitute a key source of support for this mechanism, but
it is unclear to what extent this hormone-behavior linkage
extends to the primate order. In a preregistered experiment,
we test if oxytocin receptor blockade affects affiliative
behavior in mixed-sex pairs of Eulemur, a genus of
strepsirrhine primate containing both monogamous and
non-monogamous species. Inconsistent with past studies in
monogamous voles or monkeys, we do not find confirmatory
evidence in Eulemur that monogamous pairs affiliate more
than non-monogamous pairs, nor that oxytocin receptor
blockade of one pair member selectively corresponds to
reduced affiliative or scent-marking behavior in monogamous
species. We do, however, find exploratory evidence of a
pattern not previously investigated: simultaneously blocking
oxytocin receptors in both members of a monogamous pair
predicts lower rates of affiliative behavior relative to
controls. Our study demonstrates the value of
non-traditional animal models in challenging generalizations
based on model organisms, and of methodological reform in
providing a potential path forward for behavioral oxytocin
research.},
Doi = {10.1016/j.psyneuen.2023.106044},
Key = {fds369332}
}
@article{fds368510,
Author = {Bornbusch, SL and Clarke, TA and Hobilalaina, S and Reseva, HS and LaFleur, M and Drea, CM},
Title = {Microbial rewilding in the gut microbiomes of captive
ring-tailed lemurs (Lemur catta) in Madagascar.},
Journal = {Scientific reports},
Volume = {12},
Number = {1},
Pages = {22388},
Year = {2022},
Month = {December},
url = {http://dx.doi.org/10.1038/s41598-022-26861-0},
Abstract = {Microbial rewilding, whereby exposure to naturalistic
environments can modulate or augment gut microbiomes and
improve host-microbe symbiosis, is being harnessed as
an innovative approach to human health, one that may also
have significant value to animal care and conservation. To
test for microbial rewilding in animal microbiomes, we used
a unique population of wild-born ring-tailed lemurs (Lemur
catta) that were initially held as illegal pets in unnatural
settings and, subsequently, relocated to a rescue center in
Madagascar where they live in naturalistic environments.
Using amplicon and shotgun metagenomic sequencing of lemur
and environmental microbiomes, we found multiple lines of
evidence for microbial rewilding in lemurs that were
transitioned from unnatural to naturalistic environments: A
lemur's duration of exposure to naturalistic settings
significantly correlated with (a) increased compositional
similarly to the gut communities of wild lemurs, (b)
decreased proportions of antibiotic resistance genes that
were likely acquired via human contact during pethood, and
(c) greater covariation with soil microbiomes from natural
habitats. Beyond the inherent psychosocial value of
naturalistic environments, we find that actions, such as
providing appropriate diets, minimizing contact with humans,
and increasing exposure to natural environmental consortia,
may assist in maximizing host-microbe symbiosis in animals
under human care.},
Doi = {10.1038/s41598-022-26861-0},
Key = {fds368510}
}
@article{fds365595,
Author = {Drea, CM and Davies, CS},
Title = {Meerkat manners: Endocrine mediation of female dominance and
reproductive control in a cooperative breeder.},
Journal = {Hormones and behavior},
Volume = {145},
Pages = {105245},
Year = {2022},
Month = {September},
url = {http://dx.doi.org/10.1016/j.yhbeh.2022.105245},
Abstract = {This article is part of a Special Issue (Hormones and
Hierarchies). To gain more balanced understanding of sexual
selection and mammalian sexual differentiation processes,
this review addresses behavioral sex differences and
hormonal mediators of intrasexual competition in the meerkat
(Suricata suricatta) - a cooperative breeder unusual among
vertebrates in its female aggression, degree of reproductive
skew, and phenotypic divergence. Focused on the evolution,
function, mechanism, and development of female dominance,
the male remains a key reference point throughout.
Integrated review of endocrine function does not support
routine physiological suppression in subordinates of either
sex, but instead a ramp up of weight, reproduction,
aggression, and sex steroids, particularly androgens, in
dominant females. Important and timely questions about
female competition are thus addressed by shifting emphasis
from mediators of reproductive suppression to mediators of
reproductive control, and from organizational and
activational roles of androgens in males to their roles in
females. Unusually, we ask not only how inequity is
maintained, but how dominance is acquired within a lifetime
and across generations. Antiandrogens administered in the
field to males and pregnant dominant females confirm the
importance of androgen-mediated food competition. Moreover,
effects of maternal endocrine milieu on offspring
development reveal a heritable, androgenic route to female
aggression, likely promoting reproductive priority along
dominant matrilines. Integrating endocrine measures with
long-term behavioral, ecological, morphological, and
life-history data on normative and experimental individuals,
across life stages and generations, provides better
appreciation of the role of naturally circulating androgens
in regulating the female phenotype, and sheds new light on
the evolution of female dominance, reproductive inequity,
and cooperative breeding.},
Doi = {10.1016/j.yhbeh.2022.105245},
Key = {fds365595}
}
@article{fds371301,
Author = {Bornbusch, SL and Greene, LK and Rahobilalaina, S and Calkins, S and Rothman, RS and Clarke, TA and LaFleur, M and Drea,
CM},
Title = {Gut microbiota of ring-tailed lemurs (Lemur catta) vary
across natural and captive populations and correlate with
environmental microbiota.},
Journal = {Animal microbiome},
Volume = {4},
Number = {1},
Pages = {29},
Year = {2022},
Month = {April},
url = {http://dx.doi.org/10.1186/s42523-022-00176-x},
Abstract = {<h4>Background</h4>Inter-population variation in
host-associated microbiota reflects differences in the
hosts' environments, but this characterization is typically
based on studies comparing few populations. The diversity of
natural habitats and captivity conditions occupied by any
given host species has not been captured in these
comparisons. Moreover, intraspecific variation in gut
microbiota, generally attributed to diet, may also stem from
differential acquisition of environmental microbes-an
understudied mechanism by which host microbiomes are
directly shaped by environmental microbes. To more
comprehensively characterize gut microbiota in an
ecologically flexible host, the ring-tailed lemur (Lemur
catta; n = 209), while also investigating the role of
environmental acquisition, we used 16S rRNA sequencing of
lemur gut and soil microbiota sampled from up to 13
settings, eight in the wilderness of Madagascar and five in
captivity in Madagascar or the U.S. Based on matched fecal
and soil samples, we used microbial source tracking to
examine covariation between the two types of
consortia.<h4>Results</h4>The diversity of lemur gut
microbes varied markedly within and between settings.
Microbial diversity was not consistently greater in wild
than in captive lemurs, indicating that this metric is not
necessarily an indicator of host habitat or environmental
condition. Variation in microbial composition was
inconsistent both with a single, representative gut
community for wild conspecifics and with a universal 'signal
of captivity' that homogenizes the gut consortia of captive
animals. Despite the similar, commercial diets of captive
lemurs on both continents, lemur gut microbiomes within
Madagascar were compositionally most similar, suggesting
that non-dietary factors govern some of the variability. In
particular, soil microbial communities varied across
geographic locations, with the few samples from different
continents being the most distinct, and there was
significant and context-specific covariation between gut and
soil microbiota.<h4>Conclusions</h4>As one of the broadest,
single-species investigations of primate microbiota, our
study highlights that gut consortia are sensitive to
multiple scales of environmental differences. This finding
begs a reevaluation of the simple 'captive vs. wild'
dichotomy. Beyond the important implications for animal
care, health, and conservation, our finding that
environmental acquisition may mediate aspects of
host-associated consortia further expands the framework for
how host-associated and environmental microbes interact
across different microbial landscapes.},
Doi = {10.1186/s42523-022-00176-x},
Key = {fds371301}
}
@article{fds361760,
Author = {Grebe, NM and Sheikh, A and Drea, CM},
Title = {Integrating the female masculinization and challenge
hypotheses: Female dominance, male deference, and seasonal
hormone fluctuations in adult blue-eyed black lemurs
(Eulemur flavifrons).},
Journal = {Hormones and behavior},
Volume = {139},
Pages = {105108},
Year = {2022},
Month = {March},
url = {http://dx.doi.org/10.1016/j.yhbeh.2022.105108},
Abstract = {In the decades since female social dominance was first
described in strepsirrhine primates, researchers have sought
to uncover the proximate and ultimate explanations for its
development. In the females of various female-dominant
species, androgens have been implicated as regulators of
behavior and/or predictors of seasonal fluctuations in
aggression (the 'Female Masculinization Hypothesis'). Males,
more generally, respond to changing social demands via
seasonal fluctuations in androgen-mediated behavior (the
'Challenge Hypothesis'), that may also entail changes in
activation of the hypothalamic-pituitary-adrenal axis. Here,
we explore if androgens, glucocorticoids, and intersexual
behavior fluctuate seasonally in the female-dominant,
blue-eyed black lemur (Eulemur flavifrons), with potential
consequences for understanding female aggression and male
deference. Across two studies conducted during the breeding
and nonbreeding seasons, we assessed rates of mixed-sex,
dyadic social behavior (aggression and affiliation) and
concentrations of fecal glucocorticoid metabolites (Study 1)
and serum sex hormones (androstenedione, testosterone, and
estradiol; Study 2). Our results align with several
predictions inspired by the Female Masculinization and
Challenge Hypotheses for intersexual relations: During the
breeding season, specifically, both aggression and
androstenedione peaked in females, while female-initiated
affiliation decreased, potentially to facilitate female
resource access and reproductive control. By comparison, all
target hormones (androgens, estrogen, and glucocorticoids)
peaked in males, with glucocorticoid concentrations
potentially increasing in response to the surge in female
aggression, and unusually high estrogen concentrations
year-round potentially facilitating male deference via
male-initiated affiliation. These results suggest complex,
seasonally and hormonally mediated behavior in Eulemur
flavifrons.},
Doi = {10.1016/j.yhbeh.2022.105108},
Key = {fds361760}
}
@article{fds359811,
Author = {Greene, LK and Rambeloson, E and Rasoanaivo, HA and Foss, ED and Yoder,
AD and Drea, CM and Blanco, MB},
Title = {Gut Microbial Diversity and Ecological Specialization in
Four Sympatric Lemur Species Under Lean Conditions},
Journal = {International Journal of Primatology},
Volume = {42},
Number = {6},
Pages = {961-979},
Year = {2021},
Month = {December},
url = {http://dx.doi.org/10.1007/s10764-021-00257-9},
Abstract = {The gut microbiome is gaining recognition for its role in
primate nutrition, but we stand to benefit from microbiome
comparisons across diverse hosts and environmental
conditions. We compared gut microbiome structure in four
lemur species from four phylogenetic lineages, including 9
individual mouse lemurs (Microcebus danfossi), 6 brown
lemurs (Eulemur fulvus), 20 sifakas (Propithecus coquereli),
and a single sportive lemur (Lepilemur grewcockorum). In
northwestern Madagascar, these species are sympatric, but
use different feeding strategies to cope with environmental
challenges, including relying on tree gums and insects
(mouse lemurs), and some vs. significant leaf matter (brown
lemurs vs. sifakas and sportive lemurs). From one fecal
sample collected per lemur in the dry season in the Anjajavy
Forest, we determined gut microbiome diversity, variability,
and membership via 16S rRNA sequencing. The lemurs harbored
strongly species-specific gut microbiomes. Brown lemurs
showed more diverse and generalized consortia; mouse lemurs,
sifakas, and the sportive lemur had less diverse consortia
with more distinct memberships. Consistent with their
fallback foods, mouse lemur microbiomes included taxa
putatively associated with gum and insect digestion, whereas
those of sifakas and the sportive lemur showed stronger and
distinct signatures of leaf fiber and secondary compound
metabolism. These results point to feeding strategy,
intertwined with host phylogeny, as a driver of gut
microbiome composition, but highlight real-time dietary
specificity as a contributing driver of microbiome
diversity. While illuminating how gut microbiomes facilitate
host nutrition on challenging foods, these results help
explain how ecologically diverse primates living in sympatry
may differentially cope with seasonal or stochastic lean
times.},
Doi = {10.1007/s10764-021-00257-9},
Key = {fds359811}
}
@article{fds361186,
Author = {Drea, CM and Davies, CS and Greene, LK and Mitchell, J and Blondel, DV and Shearer, CL and Feldblum, JT and Dimac-Stohl, KA and Smyth-Kabay, KN and Clutton-Brock, TH},
Title = {An intergenerational androgenic mechanism of female
intrasexual competition in the cooperatively breeding
meerkat.},
Journal = {Nature communications},
Volume = {12},
Number = {1},
Pages = {7332},
Year = {2021},
Month = {December},
url = {http://dx.doi.org/10.1038/s41467-021-27496-x},
Abstract = {Female intrasexual competition can be intense in
cooperatively breeding species, with some dominant breeders
(matriarchs) limiting reproduction in subordinates via
aggression, eviction or infanticide. In males, such
tendencies bidirectionally link to testosterone, but in
females, there has been little systematic investigation of
androgen-mediated behaviour within and across generations.
In 22 clans of wild meerkats (Suricata suricatta), we show
that matriarchs 1) express peak androgen concentrations
during late gestation, 2) when displaying peak feeding
competition, dominance behaviour, and evictions, and 3)
relative to subordinates, produce offspring that are more
aggressive in early development. Late-gestation antiandrogen
treatment of matriarchs 4) specifically reduces dominance
behaviour, is associated with infrequent evictions,
decreases social centrality within the clan, 5) increases
aggression in cohabiting subordinate dams, and 6) reduces
offspring aggression. These effects implicate
androgen-mediated aggression in the operation of female
sexual selection, and intergenerational transmission of
masculinised phenotypes in the evolution of meerkat
cooperative breeding.},
Doi = {10.1038/s41467-021-27496-x},
Key = {fds361186}
}
@article{fds359514,
Author = {Bornbusch, SL and Harris, RL and Grebe, NM and Roche, K and Dimac-Stohl,
K and Drea, CM},
Title = {Antibiotics and fecal transfaunation differentially affect
microbiota recovery, associations, and antibiotic resistance
in lemur guts.},
Journal = {Animal microbiome},
Volume = {3},
Number = {1},
Pages = {65},
Year = {2021},
Month = {October},
url = {http://dx.doi.org/10.1186/s42523-021-00126-z},
Abstract = {<h4>Background</h4>Antibiotics alter the diversity,
structure, and dynamics of host-associated microbial
consortia, including via development of antibiotic
resistance; however, patterns of recovery from microbial
imbalances and methods to mitigate associated negative
effects remain poorly understood, particularly outside of
human-clinical and model-rodent studies that focus on
outcome over process. To improve conceptual understanding of
host-microbe symbiosis in more naturalistic contexts, we
applied an ecological framework to a non-traditional,
strepsirrhine primate model via long-term, multi-faceted
study of microbial community structure before, during, and
following two experimental manipulations. Specifically, we
administered a broad-spectrum antibiotic, either alone or
with subsequent fecal transfaunation, to healthy, male
ring-tailed lemurs (Lemur catta), then used 16S rRNA and
shotgun metagenomic sequencing to longitudinally track the
diversity, composition, associations, and resistomes of
their gut microbiota both within and across baseline,
treatment, and recovery phases.<h4>Results</h4>Antibiotic
treatment resulted in a drastic decline in microbial
diversity and a dramatic alteration in community
composition. Whereas microbial diversity recovered rapidly
regardless of experimental group, patterns of microbial
community composition reflected long-term instability
following treatment with antibiotics alone, a pattern that
was attenuated by fecal transfaunation. Covariation analysis
revealed that certain taxa dominated bacterial associations,
representing potential keystone species in lemur gut
microbiota. Antibiotic resistance genes, which were
universally present, including in lemurs that had never been
administered antibiotics, varied across individuals and
treatment groups.<h4>Conclusions</h4>Long-term, integrated
study post antibiotic-induced microbial imbalance revealed
differential, metric-dependent evidence of recovery, with
beneficial effects of fecal transfaunation on recovering
community composition, and potentially negative consequences
to lemur resistomes. Beyond providing new perspectives on
the dynamics that govern host-associated communities,
particularly in the Anthropocene era, our holistic study in
an endangered species is a first step in addressing the
recent, interdisciplinary calls for greater integration of
microbiome science into animal care and conservation.},
Doi = {10.1186/s42523-021-00126-z},
Key = {fds359514}
}
@article{fds359087,
Author = {Bornbusch, SL and Drea, CM},
Title = {Antibiotic Resistance Genes in Lemur Gut and Soil Microbiota
Along a Gradient of Anthropogenic Disturbance},
Journal = {Frontiers in Ecology and Evolution},
Volume = {9},
Year = {2021},
Month = {August},
url = {http://dx.doi.org/10.3389/fevo.2021.704070},
Abstract = {The overuse of man-made antibiotics has facilitated the
global propagation of antibiotic resistance genes in
animals, across natural and anthropogenically disturbed
environments. Although antibiotic treatment is the most
well-studied route by which resistance genes can develop and
spread within host-associated microbiota, resistomes also
can be acquired or enriched via more indirect routes, such
as via transmission between hosts or via contact with
antibiotic-contaminated matter within the environment.
Relatively little is known about the impacts of
anthropogenic disturbance on reservoirs of resistance genes
in wildlife and their environments. We therefore tested for
(a) antibiotic resistance genes in primate hosts
experiencing different severities and types of anthropogenic
disturbance (i.e., non-wildlife animal presence, human
presence, direct human contact, and antibiotic treatment),
and (b) covariation between host-associated and
environmental resistomes. We used shotgun metagenomic
sequencing of ring-tailed lemur (Lemur catta) gut resistomes
and associated soil resistomes sampled from up to 10 sites:
seven in the wilderness of Madagascar and three in captivity
in Madagascar or the United States. We found that, compared
to wild lemurs, captive lemurs harbored greater abundances
of resistance genes, but not necessarily more diverse
resistomes. Abundances of resistance genes were positively
correlated with our assessments of anthropogenic
disturbance, a pattern that was robust across all ten lemur
populations. The composition of lemur resistomes was
site-specific and the types of resistance genes reflected
antibiotic usage in the country of origin, such as
vancomycin use in Madagascar. We found support for multiple
routes of ARG enrichment (e.g., via human contact,
antibiotic treatment, and environmental acquisition) that
differed across lemur populations, but could result in
similar degrees of enrichment. Soil resistomes varied across
natural habitats in Madagascar and, at sites with greater
anthropogenic disturbance, lemurs and soil resistomes
covaried. As one of the broadest, single-species
investigations of wildlife resistomes to date, we show that
the transmission and enrichment of antibiotic resistance
genes varies across environments, thereby adding to the
mounting evidence that the resistance crisis extends outside
of traditional clinical settings.},
Doi = {10.3389/fevo.2021.704070},
Key = {fds359087}
}
@article{fds371302,
Author = {Greene, LK and Blanco, MB and Rambeloson, E and Graubics, K and Fanelli,
B and Colwell, RR and Drea, CM},
Title = {Gut microbiota of frugo-folivorous sifakas across
environments.},
Journal = {Animal microbiome},
Volume = {3},
Number = {1},
Pages = {39},
Year = {2021},
Month = {May},
url = {http://dx.doi.org/10.1186/s42523-021-00093-5},
Abstract = {<h4>Background</h4>Captive animals, compared to their wild
counterparts, generally harbor imbalanced gut microbiota
owing, in part, to their altered diets. This imbalance is
particularly striking for folivores that fundamentally rely
on gut microbiota for digestion, yet rarely receive
sufficient dietary fiber in captivity. We examine the
critically endangered Coquerel's sifaka (Propithecus
coquereli), an anatomically specialized, rather than
facultative, folivore that consumes a seasonal
frugo-folivorous diet in the wild, but is provisioned
predominantly with seasonal foliage and orchard vegetables
in captivity. Using amplicon and metagenomic sequencing
applied to fecal samples collected from two wild and one
captive population (each comprising multiple groups), we
clarify how dietary variation underlies the perturbational
effect of captivity on the structure and function of this
species' gut microbiota.<h4>Results</h4>The gut microbiota
of wild sifakas varied by study population, most notably in
community evenness and in the abundance of diet-associated
microbes from Prevotellaeceae and Lachnospiraceae.
Nevertheless, the differences among wild subjects were minor
compared to those evident between wild and captive sifakas:
Unusually, the consortia of captive sifakas were the most
diverse, but lacked representation of endemic Bacteroidetes
and metagenomic capacity for essential amino-acid
biosynthesis. Instead, they were enriched for complex fiber
metabolizers from the Firmicutes phylum, for archaeal
methanogens, and for several metabolic pathways putatively
linked to plant fiber and secondary compound
metabolism.<h4>Conclusions</h4>The relatively minor
differences in gut microbial structure and function between
wild sifaka populations likely reflect regional and/or
temporal environmental variability, whereas the major
differences observed in captive conspecifics, including
the loss of endemic microbes, but gain in low-abundance
taxa, likely reflect imbalanced or unstable consortia.
Indeed, community perturbation may not necessarily entail
decreased community diversity. Moreover, signatures of
greater fiber degradation indicate that captive sifakas
consume a more fibrous diet compared to their wild
counterparts. These results do not mirror those typically
reported for folivores and herbivores, suggesting that the
direction and strength of captivity-induced 'dysbiosis' may
not be universal across species with similar feeding
strategies. We propose that tailored, species-specific
dietary interventions in captivity, aimed at better
approximating naturally foraged diets, could functionally
'rewild' gut microbiota and facilitate successful management
of diverse species.},
Doi = {10.1186/s42523-021-00093-5},
Key = {fds371302}
}
@article{fds355324,
Author = {Grebe, NM and Sharma, A and Freeman, SM and Palumbo, MC and Patisaul,
HB and Bales, KL and Drea, CM},
Title = {Neural correlates of mating system diversity: oxytocin and
vasopressin receptor distributions in monogamous and
non-monogamous Eulemur.},
Journal = {Scientific reports},
Volume = {11},
Number = {1},
Pages = {3746},
Year = {2021},
Month = {February},
url = {http://dx.doi.org/10.1038/s41598-021-83342-6},
Abstract = {Contemporary theory that emphasizes the roles of oxytocin
and vasopressin in mammalian sociality has been shaped by
seminal vole research that revealed interspecific variation
in neuroendocrine circuitry by mating system. However,
substantial challenges exist in interpreting and translating
these rodent findings to other mammalian groups, including
humans, making research on nonhuman primates crucial. Both
monogamous and non-monogamous species exist within Eulemur,
a genus of strepsirrhine primate, offering a rare
opportunity to broaden a comparative perspective on oxytocin
and vasopressin neurocircuitry with increased evolutionary
relevance to humans. We performed oxytocin and arginine
vasopressin 1a receptor autoradiography on 12 Eulemur brains
from seven closely related species to (1) characterize
receptor distributions across the genus, and (2) examine
differences between monogamous and non-monogamous species in
regions part of putative "pair-bonding circuits". We find
some binding patterns across Eulemur reminiscent of
olfactory-guided rodents, but others congruent with more
visually oriented anthropoids, consistent with lemurs
occupying an 'intermediary' evolutionary niche between
haplorhine primates and other mammalian groups. We find
little evidence of a "pair-bonding circuit" in Eulemur akin
to those proposed in previous rodent or primate research.
Mapping neuropeptide receptors in these nontraditional
species questions existing assumptions and informs proposed
evolutionary explanations about the biological bases of
monogamy.},
Doi = {10.1038/s41598-021-83342-6},
Key = {fds355324}
}
@article{fds353245,
Author = {Drea, CM and Crawford, JC and Boulet, M},
Title = {Lack of evidence for pheromones in lemurs.},
Journal = {Current biology : CB},
Volume = {30},
Number = {22},
Pages = {R1355-R1357},
Year = {2020},
Month = {November},
url = {http://dx.doi.org/10.1016/j.cub.2020.10.005},
Abstract = {As chemicals that elicit unlearned, functionally
specialized, and species-specific responses [1] or
'stereotyped behavior' [2], pheromones differ from mammalian
scent signatures that comprise complex, variable mixtures,
convey multiple messages via learned chemical combinations,
and elicit generalized responses [1]. Studying ring-tailed
lemur (Lemur catta) behavior and semiochemistry, a recent
study by Shirasu, Ito et al. [2] claimed to have identified
"the first sex pheromones in primates." However, reliance on
one male in most chemical procedures and on few females in
behavioral procedures constrains statistical analyses and
challenges the broad applicability of their findings. Also,
the non-independent testing of even fewer signaler-recipient
dyads downplays the critical role of learning and memory in
primate communication [1] - an argument that refuted earlier
claims of primate pheromones [3,4]. Here, we challenge each
of their four highlighted findings and interpretations.},
Doi = {10.1016/j.cub.2020.10.005},
Key = {fds353245}
}
@article{fds352328,
Author = {Conley, A and Place, NJ and Legacki, EL and Hammond, GL and Cunha, GR and Drea, CM and Weldele, ML and Glickman, SE},
Title = {Spotted hyaenas and the sexual spectrum: reproductive
endocrinology and development.},
Journal = {The Journal of endocrinology},
Volume = {247},
Number = {1},
Pages = {R27-R44},
Year = {2020},
Month = {October},
url = {http://dx.doi.org/10.1530/joe-20-0252},
Abstract = {The spotted hyaena (Crocuta crocuta) is a unique species,
even amongst the Hyaenidae. Extreme clitoral development in
female spotted hyaenas challenges aspects of the accepted
framework of sexual differentiation and reproductive
function. They lack a vulva and instead urinate, copulate
and give birth through a single, long urogenital canal that
traverses a clitoris superficially resembling a penis.
Recent and historical evidence is reviewed to describe our
changing understanding of the biology of this species.
Expanding upon observations from hyaenas in nature, much has
been learned from studies utilising the captive colony at
the University of California, Berkeley. The steroid
environment of pregnancy is shaped by placental androgen and
oestrogen secretion and a late gestational increase in sex
hormone binding globulin, the regulated expression and
steroid-binding characteristics of which are unique within
the Hyaenidae. While initial external genital development is
largely free of androgenic influence, the increase in
testosterone concentrations in late gestation influences
foetal development. Specifically, anti-androgen (AA)
treatment of pregnant females reduced the developmental
influence of androgens on their foetuses, resulting in
reduced androstenedione concentrations in young females and
easier birth through a 'feminised' clitoris, but precluded
intromission and mating by 'feminised' male offspring, and
altered social interactions. Insight into the costs and
benefits of androgen exposure on spotted hyaena reproductive
development, endocrinology and behaviour emphasises the
delicate balance that sustains reproductive success, forces
a re-evaluation of how we define masculine vs feminine
sexual characteristics, and motivates reflection about the
representative value of model species.},
Doi = {10.1530/joe-20-0252},
Key = {fds352328}
}
@article{fds349325,
Author = {Greene, LK and Williams, CV and Junge, RE and Mahefarisoa, KL and Rajaonarivelo, T and Rakotondrainibe, H and O'Connell, TM and Drea,
CM},
Title = {A role for gut microbiota in host niche differentiation.},
Journal = {The ISME journal},
Volume = {14},
Number = {7},
Pages = {1675-1687},
Year = {2020},
Month = {July},
url = {http://dx.doi.org/10.1038/s41396-020-0640-4},
Abstract = {If gut microbes influence host behavioral ecology in the
short term, over evolutionary time, they could drive host
niche differentiation. We explored this possibility by
comparing the gut microbiota of Madagascar's folivorous
lemurs from Indriidae and Lepilemuridae. Occurring
sympatrically in the eastern rainforest, our four, target
species have different dietary specializations, including
frugo-folivory (sifakas), young-leaf folivory (indri and
woolly lemurs), and mature-leaf folivory (sportive lemurs).
We collected fecal samples, from 2013 to 2017, and used
amplicon sequencing, metagenomic sequencing, and nuclear
magnetic resonance spectroscopy, respectively, to integrate
analyses of gut microbiome structure and function with
analysis of the colonic metabolome. The lemurs harbored
species-specific microbiomes, metagenomes, and metabolomes
that were tuned to their dietary specializations:
Frugo-folivores had greater microbial and metagenomic
diversity, and harbored generalist taxa. Mature-leaf
folivores had greater individual microbiome variation, and
taxa and metabolites putatively involved in cellulolysis.
The consortia even differed between related, young-leaf
specialists, with indri prioritizing metabolism of fiber and
plant secondary compounds, and woolly lemurs prioritizing
amino-acid cycling. Specialized gut microbiota and
associated gastrointestinal morphologies enable folivores to
variably tolerate resource fluctuation and support nutrient
extraction from challenging resources (e.g., by metabolizing
plant secondary compounds or recalcitrant fibers), perhaps
ultimately facilitating host species' diversity and
specialized feeding ecologies.},
Doi = {10.1038/s41396-020-0640-4},
Key = {fds349325}
}
@article{fds349883,
Author = {Drea, CM},
Title = {Design, delivery and perception of condition-dependent
chemical signals in strepsirrhine primates: implications for
human olfactory communication.},
Journal = {Philosophical transactions of the Royal Society of London.
Series B, Biological sciences},
Volume = {375},
Number = {1800},
Pages = {20190264},
Year = {2020},
Month = {June},
url = {http://dx.doi.org/10.1098/rstb.2019.0264},
Abstract = {The study of human chemical communication benefits from
comparative perspectives that relate humans, conceptually
and empirically, to other primates. All major primate groups
rely on intraspecific chemosignals, but strepsirrhines
present the greatest diversity and specialization, providing
a rich framework for examining design, delivery and
perception. Strepsirrhines actively scent mark, possess a
functional vomeronasal organ, investigate scents via
olfactory and gustatory means, and are exquisitely sensitive
to chemically encoded messages. Variation in delivery, scent
mixing and multimodality alters signal detection, longevity
and intended audience. Based on an integrative, 19-species
review, the main scent source used (excretory versus
glandular) differentiates nocturnal from diurnal or
cathemeral species, reflecting differing socioecological
demands and evolutionary trajectories. Condition-dependent
signals reflect immutable (species, sex, identity, genetic
diversity, immunity and kinship) and transient (health,
social status, reproductive state and breeding history)
traits, consistent with socio-reproductive functions. Sex
reversals in glandular elaboration, marking rates or
chemical richness in female-dominant species implicate
sexual selection of olfactory ornaments in both sexes.
Whereas some compounds may be endogenously produced and
modified (e.g. via hormones), microbial analyses of
different odorants support the fermentation hypothesis of
bacterial contribution. The intimate contexts of information
transfer and varied functions provide important parallels
applicable to olfactory communication in humans. This
article is part of the Theo Murphy meeting issue 'Olfactory
communication in humans'.},
Doi = {10.1098/rstb.2019.0264},
Key = {fds349883}
}
@article{fds349884,
Author = {Bornbusch, SL and Grebe, NM and Lunn, S and Southworth, CA and Dimac-Stohl, K and Drea, C},
Title = {Stable and transient structural variation in lemur vaginal,
labial and axillary microbiomes: patterns by species, body
site, ovarian hormones and forest access.},
Journal = {FEMS microbiology ecology},
Volume = {96},
Number = {6},
Pages = {fiaa090},
Year = {2020},
Month = {June},
url = {http://dx.doi.org/10.1093/femsec/fiaa090},
Abstract = {Host-associated microbiomes shape and are shaped by myriad
processes that ultimately delineate their symbiotic
functions. Whereas a host's stable traits, such as its
lineage, relate to gross aspects of its microbiome
structure, transient factors, such as its varying
physiological state, relate to shorter term, structural
variation. Our understanding of these relationships in
primates derives principally from anthropoid studies and
would benefit from a broader, comparative perspective. We
thus examined the vaginal, labial and axillary microbiota of
captive, female ring-tailed lemurs (Lemur catta) and
Coquerel's sifakas (Propithecus coquereli), across an
ovarian cycle, to better understand their relation to stable
(e.g. species identity/mating system, body site) and
transient (e.g. ovarian hormone concentration, forest
access) host features. We used 16S amplicon sequencing to
determine microbial composition and enzyme-linked
immunosorbent assays to measure serum hormone
concentrations. We found marked variation in microbiota
diversity and community composition between lemur species
and their body sites. Across both host species, microbial
diversity was significantly correlated with ovarian hormone
concentrations: negatively with progesterone and positively
with estradiol. The hosts' differential forest access
related to the diversity of environmental microbes,
particularly in axillary microbiomes. Such transient
endogenous and exogenous modulators have potential
implications for host reproductive health and behavioral
ecology.},
Doi = {10.1093/femsec/fiaa090},
Key = {fds349884}
}
@article{fds345043,
Author = {Greene, LK and Bornbusch, SL and McKenney, EA and Harris, RL and Gorvetzian, SR and Yoder, AD and Drea, CM},
Title = {The importance of scale in comparative microbiome research:
New insights from the gut and glands of captive and wild
lemurs.},
Journal = {American journal of primatology},
Volume = {81},
Number = {10-11},
Pages = {e22974},
Year = {2019},
Month = {October},
url = {http://dx.doi.org/10.1002/ajp.22974},
Abstract = {Research on animal microbiomes is increasingly aimed at
determining the evolutionary and ecological factors that
govern host-microbiome dynamics, which are invariably
intertwined and potentially synergistic. We present three
empirical studies related to this topic, each of which
relies on the diversity of Malagasy lemurs (representing a
total of 19 species) and the comparative approach applied
across scales of analysis. In Study 1, we compare gut
microbial membership across 14 species in the wild to test
the relative importance of host phylogeny and feeding
strategy in mediating microbiome structure. Whereas host
phylogeny strongly predicted community composition, the same
feeding strategies shared by distant relatives did not
produce convergent microbial consortia, but rather shaped
microbiomes in host lineage-specific ways, particularly in
folivores. In Study 2, we compare 14 species of wild and
captive folivores, frugivores, and omnivores, to highlight
the importance of captive populations for advancing gut
microbiome research. We show that the perturbational effect
of captivity is mediated by host feeding strategy and can be
mitigated, in part, by modified animal management. In Study
3, we examine various scent-gland microbiomes across three
species in the wild or captivity and show them to vary by
host species, sex, body site, and a proxy of social status.
These rare data provide support for the bacterial
fermentation hypothesis in olfactory signal production and
implicate steroid hormones as mediators of microbial
community structure. We conclude by discussing the role of
scale in comparative microbial studies, the links between
feeding strategy and host-microbiome coadaptation, the
underappreciated benefits of captive populations for
advancing conservation research, and the need to consider
the entirety of an animal's microbiota. Ultimately, these
studies will help move the field from exploratory to
hypothesis-driven research.},
Doi = {10.1002/ajp.22974},
Key = {fds345043}
}
@article{fds345022,
Author = {Grebe, NM and Fitzpatrick, C and Sharrock, K and Starling, A and Drea,
CM},
Title = {Organizational and activational androgens, lemur social
play, and the ontogeny of female dominance.},
Journal = {Hormones and behavior},
Volume = {115},
Pages = {104554},
Year = {2019},
Month = {September},
url = {http://dx.doi.org/10.1016/j.yhbeh.2019.07.002},
Abstract = {The role of androgens in shaping "masculine" traits in males
is a core focus in behavioral endocrinology, but relatively
little is known about an androgenic role in female
aggression and social dominance. In mammalian models of
female dominance, including the ring-tailed lemur (Lemur
catta), links to androgens in adulthood are variable. We
studied the development of ring-tailed lemurs to address the
behavioral basis and ontogenetic mechanisms of female
dominance. We measured behavior and serum androgen
concentrations in 24 lemurs (8 males, 16 females) from
infancy to early adulthood, and assessed their 'prenatal'
androgen milieu using serum samples obtained from their
mothers during gestation. Because logistical constraints
limited the frequency of infant blood sampling, we accounted
for asynchrony between behavioral and postnatal hormone
measurements via imputation procedures. Imputation was
unnecessary for prenatal hormone measurements. The typical
sex difference in androgen concentrations in young lemurs
was consistent with adult conspecifics and most other
mammals; however, we found no significant sex differences in
rough-and-tumble play. Female (but not male) aggression
increased beginning at approximately 15 months, coincident
with female puberty. In our analyses relating sexually
differentiated behavior to androgens, we found no
relationship with activational hormones, but several
significant relationships with organizational hormones.
Notably, associations of prenatal androstenedione and
testosterone with behavior were differentiated, both by
offspring sex and by type of behavior within offspring
sexes. We discuss the importance of considering (1) missing
data in behavioral endocrinology research, and (2)
organizational androgens other than testosterone in studies
of female dominance.},
Doi = {10.1016/j.yhbeh.2019.07.002},
Key = {fds345022}
}
@article{fds345872,
Author = {Grogan, KE and Harris, RL and Boulet, M and Drea,
CM},
Title = {Genetic variation at MHC class II loci influences both
olfactory signals and scent discrimination in ring-tailed
lemurs.},
Journal = {BMC evolutionary biology},
Volume = {19},
Number = {1},
Pages = {171},
Year = {2019},
Month = {August},
url = {http://dx.doi.org/10.1186/s12862-019-1486-0},
Abstract = {<h4>Background</h4>Diversity at the Major Histocompatibility
Complex (MHC) is critical to health and fitness, such that
MHC genotype may predict an individual's quality or
compatibility as a competitor, ally, or mate. Moreover,
because MHC products can influence the components of bodily
secretions, an individual's body odors may signal its MHC
composition and influence partner identification or mate
choice. Here, we investigated MHC-based signaling and
recipient sensitivity by testing for odor-gene covariance
and behavioral discrimination of MHC diversity and pairwise
dissimilarity in a strepsirrhine primate, the ring-tailed
lemur (Lemur catta).<h4>Methods</h4>First, we coupled
genotyping of the MHC class II gene, DRB, with gas
chromatography-mass spectrometry of genital gland secretions
to investigate if functional genetic diversity is signaled
by the chemical diversity of lemur scent secretions. We also
assessed if the chemical similarity between individuals
correlated with their MHC-DRB similarity. Next, we assessed
if lemurs discriminated this chemically encoded, genetic
information in opposite-sex conspecifics.<h4>Results</h4>We
found that both sexes signaled overall MHC-DRB diversity and
pairwise MHC-DRB similarity via genital secretions, but in a
sex- and season-dependent manner. Additionally, the sexes
discriminated absolute and relative MHC-DRB diversity in the
genital odors of opposite-sex conspecifics, suggesting that
lemur genital odors function to advertise genetic
quality.<h4>Conclusions</h4>In summary, genital odors of
ring-tailed lemurs provide honest information about an
individual's absolute and relative MHC quality.
Complementing evidence in humans and Old World monkeys, we
suggest that reliance on scent signals to communicate MHC
quality may be important across the primate
lineage.},
Doi = {10.1186/s12862-019-1486-0},
Key = {fds345872}
}
@article{fds344714,
Author = {Greene, LK and Clayton, JB and Rothman, RS and Semel, BP and Semel, MA and Gillespie, TR and Wright, PC and Drea, CM},
Title = {Local habitat, not phylogenetic relatedness, predicts gut
microbiota better within folivorous than frugivorous lemur
lineages.},
Journal = {Biology letters},
Volume = {15},
Number = {6},
Pages = {20190028},
Year = {2019},
Month = {June},
url = {http://dx.doi.org/10.1098/rsbl.2019.0028},
Abstract = {Both host phylogenetic placement and feeding strategy
influence the structure of the gut microbiome (GMB);
however, parsing their relative contributions presents a
challenge. To meet this challenge, we compared GMB structure
in two genera of lemurs characterized by different dietary
specializations, the frugivorous brown lemurs ( Eulemur
spp.) and the folivorous sifakas ( Propithecus spp.). These
genera sympatrically occupy similar habitats (dry forests
and rainforests) and diverged over similar evolutionary
timescales. We collected fresh faeces from 12 species (six
per host genus), at seven sites across Madagascar, and
sequenced the 16S rRNA gene to determine GMB membership,
diversity and variability. The lemurs' GMBs clustered
predominantly by host genus; nevertheless, within genera,
host relatedness did not predict GMB distance between
species. The GMBs of brown lemurs had greater evenness and
diversity, but were more homogeneous across species, whereas
the GMBs of sifakas were differentiated between habitats.
Thus, over relatively shallow timescales, environmental
factors can override the influence of host phylogenetic
placement on GMB phylogenetic composition. Moreover, feeding
strategy can underlie the relative strength of
host-microbiome coadaptation, with Madagascar's folivores
perhaps requiring locally adapted GMBs to facilitate their
highly specialized diets.},
Doi = {10.1098/rsbl.2019.0028},
Key = {fds344714}
}
@article{fds345044,
Author = {Bornbusch, SL and Greene, LK and Harris, RL and Drea,
CM},
Title = {Glandular microbiomes vary by species and host traits in
wild and captive lemurs},
Journal = {AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY},
Volume = {168},
Pages = {25-25},
Publisher = {WILEY},
Year = {2019},
Month = {March},
Key = {fds345044}
}
@article{fds366269,
Author = {Drea, CM and Goodwin, TE and delBarco-Trillo, J},
Title = {P-Mail: The Information Highway of Nocturnal, but Not
Diurnal or Cathemeral, Strepsirrhines.},
Journal = {Folia primatologica; international journal of
primatology},
Volume = {90},
Number = {5},
Pages = {422-438},
Year = {2019},
Month = {January},
url = {http://dx.doi.org/10.1159/000495076},
Abstract = {Scent marking is a well-established, but highly variable,
mode of communication among strepsirrhine primates. We begin
by reviewing this literature, focusing on nocturnal species.
Our understanding about the information content of scent
signals and the factors driving species diversity remains
incomplete, owing to difficulties in acquiring comparative
chemical data. We therefore re-examine such a data set,
representing the richness and relative abundance of volatile
organic compounds (VOCs) in the urine of 12 species (from
Galagidae, Lorisidae, Daubentoniidae, Cheirogaleidae,
Indriidae, and Lemuridae), to explore differences between
nocturnal, diurnal and cathemeral species. As predicted by
the variable importance of urine marking across species, the
urine of nocturnal strepsirrhines contained the most VOCs
and putative semiochemicals, differed significantly in
composition from that of diurnal and cathemeral species and
showed the strongest species scent "signatures." Relevant to
retracing the evolutionary trajectory of cathemeral
strepsirrhines, nocturnal and diurnal species were most
differentiated in their VOCs, with cathemeral species being
intermediary, but more closely aligned with diurnal species.
These data support cathemerality as an ancient expansion of
diurnal animals into a nocturnal niche. Consideration of the
traits and variables associated with olfactory communication
offers a profitable new way for examining species diversity
and patterns of evolutionary change.},
Doi = {10.1159/000495076},
Key = {fds366269}
}
@article{fds338472,
Author = {Greene, LK and McKenney, EA and O'Connell, TM and Drea,
CM},
Title = {The critical role of dietary foliage in maintaining the gut
microbiome and metabolome of folivorous sifakas.},
Journal = {Scientific reports},
Volume = {8},
Number = {1},
Pages = {14482},
Year = {2018},
Month = {September},
url = {http://dx.doi.org/10.1038/s41598-018-32759-7},
Abstract = {The gut microbiome (GMB) of folivores metabolizes dietary
fiber into nutrients, including short-chain fatty acids
(SCFAs); however, experiments probing the consequences of
foliage quality on host GMBs are lacking. We therefore
examined GMB structure and function via amplicon sequencing
and Nuclear Magnetic Resonance spectroscopy in 31 captive
sifakas (Propithecus coquereli) during dietary manipulations
associated with husbandry. Supplementing standard diets with
diverse foliage blends, versus with a single plant species,
promoted more diverse GMBs, enriched for taxa implicated in
plant-fiber metabolism, but depleted in taxa implicated in
starch metabolism and bile tolerance. The consumption of
diverse blends was associated with greater concentrations of
colonic SCFAs. Abundant foliage, via forest access, promoted
compositionally distinct and more stable GMBs, but reduced
concentrations of SCFAs, possibly reflecting selection of
high-quality leaves. In 11 subjects denied forest access, we
examined the temporal pace of microbial shifts when
supplemental foliage was abruptly switched between diverse
blends and single species. The sifaka GMB responded within
days, with community diversity and composition closely
tracking foliage diversity. By providing experimental
evidence that the folivore GMB is sensitive to minor changes
in dietary foliage, we reveal the fragility of specialist
GMBs, with implications for managing the wellbeing of
endangered wildlife.},
Doi = {10.1038/s41598-018-32759-7},
Key = {fds338472}
}
@article{fds335470,
Author = {Dimac-Stohl, KA and Davies, CS and Grebe, NM and Stonehill, AC and Greene, LK and Mitchell, J and Clutton-Brock, T and Drea,
CM},
Title = {Incidence and biomarkers of pregnancy, spontaneous abortion,
and neonatal loss during an environmental stressor:
Implications for female reproductive suppression in the
cooperatively breeding meerkat.},
Journal = {Physiology & behavior},
Volume = {193},
Number = {Pt A},
Pages = {90-100},
Year = {2018},
Month = {September},
url = {http://dx.doi.org/10.1016/j.physbeh.2017.11.011},
Abstract = {Meerkats are group-living, insectivorous herpestids in which
subordinate members provide extensive care for the dominant
female's young. In contrast to some cooperative breeders,
subordinate female meerkats are physiologically able to
reproduce and occasionally do so successfully; their
attempts are more frequently 'suppressed' via eviction or
infanticide by the dominant female. Spontaneous abortion and
neonatal loss occur with some regularity, further negatively
impacting reproductive success. Here, we compared the
reproductive outcomes and endocrine profiles, including of
serum progesterone (P<sub>4</sub>), serum estradiol
(E<sub>2</sub>), and fecal glucocorticoid metabolites
(fGCm), of dominant and subordinate dams residing within
their clans in the Kalahari Desert of South Africa. Our
study spanned years of drought, which reduced insect
abundance and represented a substantial environmental
stressor. Meerkat pregnancies were identified at mid-term
and culminated either in spontaneous abortions or full-term
deliveries, after which pups were either lost prior to
emergence from the natal den (usually within 2days of birth)
or emerged at 2-3weeks. Neonatal loss exceeded fetal loss
for all females, and contributed to narrowing the
status-related disparity in female reproductive output seen
during less arid periods. Although E<sub>2</sub>
concentrations were significantly lower in subordinate than
dominant females, they were sufficient to support gestation.
Absolute E<sub>2</sub> concentrations may owe to androgenic
precursors that also attain highest concentrations in
dominant dams and may mediate aggression underlying female
reproductive skew. Pregnancies terminating in fetal loss
were marked by significantly lower P<sub>4</sub>
concentrations in mid-gestation and modestly lower
E<sub>2</sub> concentrations overall. Consistently high fGCm
concentrations further increased across trimesters,
particularly (but not consistently) in subordinates and in
aborted pregnancies. Environmental stressors may modulate
reproductive outcomes in meerkats through their influence on
sex steroids and their effects on intragroup competition.
The social and eco-physiological factors affecting
intraspecific variation in reproductive output, even in
obligate cooperative breeders, may be most apparent during
extreme conditions, reflecting the benefits of long-term
studies for assessing the impact of climate
change.},
Doi = {10.1016/j.physbeh.2017.11.011},
Key = {fds335470}
}
@article{fds338037,
Author = {Smyth, KN and Caruso, NM and Davies, CS and Clutton-Brock, TH and Drea,
CM},
Title = {Social and endocrine correlates of immune function in
meerkats: implications for the immunocompetence handicap
hypothesis.},
Journal = {Royal Society open science},
Volume = {5},
Number = {8},
Pages = {180435},
Year = {2018},
Month = {August},
url = {http://dx.doi.org/10.1098/rsos.180435},
Abstract = {Social status can mediate effects on the immune system, with
profound consequences for individual health; nevertheless,
most investigators of status-related disparities in
free-ranging animals have used faecal parasite burdens to
proxy immune function in the males of male-dominant species.
We instead use direct measures of innate immune function
(complement and natural antibodies) to examine
status-related immunocompetence in both sexes of a
female-dominant species. The meerkat is a unique model for
such a study because it is a cooperatively breeding species
in which status-related differences are extreme, evident in
reproductive skew, morphology, behaviour, communication and
physiology, including that dominant females naturally
express the greatest total androgen (androstenedione plus
testosterone) concentrations. We found that, relative to
subordinates, dominant animals had reduced serum
bacteria-killing abilities; also, relative to subordinate
females, dominant females had reduced haemolytic complement
activities. Irrespective of an individual's sex or social
status, androstenedione concentrations (but not body
condition, age or reproductive activity) negatively
predicted concurrent immunocompetence. Thus, dominant
meerkats of both sexes are immunocompromised. Moreover, in
female meerkats, androstenedione perhaps acting directly or
via local conversion, may exert a double-edged effect of
promoting dominance and reproductive success at the cost of
increased parasitism and reduced immune function. Given the
prominent signalling of dominance in female meerkats, these
findings may relate to the immunocompetence handicap
hypothesis (ICHH); however, our data would suggest that the
endocrine mechanism underlying the ICHH need not be mediated
solely by testosterone and might explain trade-offs in
females, as well as in males.},
Doi = {10.1098/rsos.180435},
Key = {fds338037}
}
@article{fds335471,
Author = {Harris, RL and Boulet, M and Grogan, KE and Drea,
CM},
Title = {Costs of injury for scent signalling in a strepsirrhine
primate.},
Journal = {Scientific reports},
Volume = {8},
Number = {1},
Pages = {9882},
Year = {2018},
Month = {June},
url = {http://dx.doi.org/10.1038/s41598-018-27322-3},
Abstract = {Honesty is crucial in animal communication when signallers
are conveying information about their condition. Condition
dependence implies a cost to signal production; yet,
evidence of such cost is scarce. We examined the effects of
naturally occurring injury on the quality and salience of
olfactory signals in ring-tailed lemurs (Lemur catta). Over
a decade, we collected genital secretions from 23 (13 male,
10 female) adults across 34 unique injuries, owing primarily
to intra-group fights. Using gas chromatography-mass
spectrometry, we tested for differences in the chemical
composition of secretions across pre-injury, injury and
recovery, in animals that did and did not receive
antibiotics. Lemur genital secretions were significantly
dampened and altered during injury, with patterns of change
varying by sex, season and antibiotics. Using behavioural
bioassays (excluding odorants from antibiotic-treated
animals), we showed that male 'recipients' discriminated
injury status based on scent alone, directing more
competitive counter marking towards odorants from injured
vs. uninjured male 'signallers.' That injured animals could
not maintain their normal signatures provides rare evidence
of the energetic cost to signal production. That
conspecifics detected olfactory-encoded 'weakness' suggests
added behavioural costs: By influencing the likelihood of
intra- or inter-sexual conflict, condition-dependent signals
could have important implications for socio-reproductive
behaviour.},
Doi = {10.1038/s41598-018-27322-3},
Key = {fds335471}
}
@article{fds345045,
Author = {Drea, CM},
Title = {Social Communication of Condition-Dependent Olfactory
Signals in Strepsirrhine Primates},
Journal = {CHEMICAL SENSES},
Volume = {43},
Number = {4},
Pages = {E7-E7},
Publisher = {OXFORD UNIV PRESS},
Year = {2018},
Month = {May},
Key = {fds345045}
}
@article{fds345046,
Author = {Gorvetzian, SR and Greene, LK and Drea, CM},
Title = {Free-ranging access improves the gut microbiome of captive
Eulemur},
Journal = {AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY},
Volume = {165},
Pages = {103-103},
Publisher = {WILEY},
Year = {2018},
Month = {April},
Key = {fds345046}
}
@article{fds345047,
Author = {Drea, CM and Goodwin, TE and Delbarco-Trillo, J},
Title = {Pee-mail: The information highway of nocturnal
strepsirrhines},
Journal = {AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY},
Volume = {165},
Pages = {71-72},
Publisher = {WILEY},
Year = {2018},
Month = {April},
Key = {fds345047}
}
@article{fds345048,
Author = {Bornbusch, SL and Greene, LK and Drea, CM},
Title = {Anthropogenic disturbance as a determinant of gut microbiome
structure in Madagascar's ring-tailed lemurs (Lemur
catta)},
Journal = {AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY},
Volume = {165},
Pages = {33-33},
Publisher = {WILEY},
Year = {2018},
Month = {April},
Key = {fds345048}
}
@article{fds345049,
Author = {Grebe, NM and Drea, CM},
Title = {Ontogeny of female dominance in ring-tailed lemurs:
behavioral and hormonal evidence},
Journal = {AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY},
Volume = {165},
Pages = {104-104},
Publisher = {WILEY},
Year = {2018},
Month = {April},
Key = {fds345049}
}
@article{fds345050,
Author = {Greene, LK and Mckenney, EA and O'Connell, TM and Drea,
CM},
Title = {Dietary foliage regulates the gut microbiome and colonic
metabolome of captive Coquerel's sifakas},
Journal = {AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY},
Volume = {165},
Pages = {105-105},
Publisher = {WILEY},
Year = {2018},
Month = {April},
Key = {fds345050}
}
@article{fds329341,
Author = {Grogan, KE and Sauther, ML and Cuozzo, FP and Drea,
CM},
Title = {Genetic wealth, population health: Major histocompatibility
complex variation in captive and wild ring-tailed lemurs
(Lemur catta).},
Journal = {Ecology and evolution},
Volume = {7},
Number = {19},
Pages = {7638-7649},
Year = {2017},
Month = {October},
url = {http://dx.doi.org/10.1002/ece3.3317},
Abstract = {Across species, diversity at the major histocompatibility
complex (MHC) is critical to individual disease resistance
and, hence, to population health; however, MHC diversity can
be reduced in small, fragmented, or isolated populations.
Given the need for comparative studies of functional genetic
diversity, we investigated whether MHC diversity differs
between populations which are open, that is experiencing
gene flow, versus populations which are closed, that is
isolated from other populations. Using the endangered
ring-tailed lemur (<i>Lemur catta</i>) as a model, we
compared two populations under long-term study: a relatively
"open," wild population (<i>n</i> = 180) derived from
Bezà Mahafaly Special Reserve, Madagascar (2003-2013) and a
"closed," captive population (<i>n</i> = 121) derived from
the Duke Lemur Center (DLC, 1980-2013) and from the
Indianapolis and Cincinnati Zoos (2012). For all animals, we
assessed MHC-DRB diversity and, across populations, we
compared the number of unique MHC-DRB alleles and their
distributions. Wild individuals possessed more MHC-DRB
alleles than did captive individuals, and overall, the wild
population had more unique MHC-DRB alleles that were more
evenly distributed than did the captive population. Despite
management efforts to maintain or increase genetic diversity
in the DLC population, MHC diversity remained static from
1980 to 2010. Since 2010, however, captive-breeding efforts
resulted in the MHC diversity of offspring increasing to a
level commensurate with that found in wild individuals.
Therefore, loss of genetic diversity in lemurs, owing to
small founder populations or reduced gene flow, can be
mitigated by managed breeding efforts. Quantifying MHC
diversity within individuals and between populations is the
necessary first step to identifying potential improvements
to captive management and conservation plans.},
Doi = {10.1002/ece3.3317},
Key = {fds329341}
}
@article{fds326999,
Author = {Leclaire, S and Jacob, S and Greene, LK and Dubay, GR and Drea,
CM},
Title = {Social odours covary with bacterial community in the anal
secretions of wild meerkats.},
Journal = {Scientific reports},
Volume = {7},
Number = {1},
Pages = {3240},
Year = {2017},
Month = {June},
url = {http://dx.doi.org/10.1038/s41598-017-03356-x},
Abstract = {The fermentation hypothesis for animal signalling posits
that bacteria dwelling in an animal's scent glands
metabolize the glands' primary products into odorous
compounds used by the host to communicate with conspecifics.
There is, however, little evidence of the predicted
covariation between an animal's olfactory cues and its
glandular bacterial communities. Using gas
chromatography-mass spectrometry, we first identified the
volatile compounds present in 'pure' versus 'mixed'
anal-gland secretions ('paste') of adult meerkats (Suricata
suricatta) living in the wild. Low-molecular-weight
chemicals that likely derive from bacterial metabolism were
more prominent in mixed than pure secretions. Focusing
thereafter on mixed secretions, we showed that chemical
composition varied by sex and was more similar between
members of the same group than between members of different
groups. Subsequently, using next-generation sequencing, we
identified the bacterial assemblages present in meerkat
paste and documented relationships between these assemblages
and the host's sex, social status and group membership.
Lastly, we found significant covariation between the
volatile compounds and bacterial assemblages in meerkat
paste, particularly in males. Together, these results are
consistent with a role for bacteria in the production of
sex- and group-specific scents, and with the evolution of
mutualism between meerkats and their glandular
microbiota.},
Doi = {10.1038/s41598-017-03356-x},
Key = {fds326999}
}
@article{fds345051,
Author = {Drea, CM},
Title = {Condition-dependent Scent Signals in Strepsirrhine
Primates},
Journal = {AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY},
Volume = {162},
Pages = {165-166},
Publisher = {WILEY},
Year = {2017},
Month = {April},
Key = {fds345051}
}
@article{fds345052,
Author = {Smyth, KN and Stonehill, A and Caruso, N and Drea,
CM},
Title = {Consequences of Prenatal Androgen Exposure for Offspring
Health: an Experimental Study in Wild Meerkats},
Journal = {INTEGRATIVE AND COMPARATIVE BIOLOGY},
Volume = {57},
Pages = {E158-E158},
Publisher = {OXFORD UNIV PRESS INC},
Year = {2017},
Month = {March},
Key = {fds345052}
}
@article{fds345053,
Author = {Harris, RL and Drea, CM},
Title = {In Sickness and In Health: Olfactory Cues of Injury and
Illness in Lemurs},
Journal = {INTEGRATIVE AND COMPARATIVE BIOLOGY},
Volume = {57},
Pages = {E284-E284},
Publisher = {OXFORD UNIV PRESS INC},
Year = {2017},
Month = {March},
Key = {fds345053}
}
@article{fds345023,
Author = {McKenney, EA and Greene, LK and Drea, CM and Yoder,
AD},
Title = {Down for the count: Cryptosporidium infection
depletes the gut microbiome in Coquerel's
sifakas.},
Journal = {Microbial ecology in health and disease},
Volume = {28},
Number = {1},
Pages = {1335165},
Year = {2017},
Month = {January},
url = {http://dx.doi.org/10.1080/16512235.2017.1335165},
Abstract = {<b>Background</b>: The gut microbiome (GMB) is the first
line of defense against enteric pathogens, which are a
leading cause of disease and mortality worldwide. One such
pathogen, the protozoan <i>Cryptosporidium</i>, causes a
variety of digestive disorders that can be devastating and
even lethal. The Coquerel's sifaka (<i>Propithecus
coquereli</i>) - an endangered, folivorous primate endemic
to Madagascar - is precariously susceptible to
cryptosporidiosis under captive conditions. If left
untreated, infection can rapidly advance to morbidity and
death. <b>Objective</b>: To gain a richer understanding of
the pathophysiology of this pathogen while also improving
captive management of endangered species, we examine the
impact of cryptosporidiosis on the GMB of a flagship species
known to experience a debilitating disease state upon
infection. <b>Design</b>: Using 16S sequencing of DNA
extracted from sifaka fecal samples, we compared the
microbial communities of healthy sifakas to those of
infected individuals, across infection and recovery periods.
<b>Results</b>: Over the course of infection, we found that
the sifaka GMB responds with decreased microbial diversity
and increased community dissimilarity. Compared to the GMB
of unaffected individuals, as well as during pre-infection
and recovery periods, the GMB during active infection was
enriched for microbial taxa associated with dysbiosis and
rapid transit time. Time to recovery was inversely related
to age, with young animals being slowest to recover GMB
diversity and full community membership. Antimicrobial
treatment during infection caused a significant depletion in
GMB diversity. <b>Conclusions</b>: Although individual
sifakas show unique trajectories of microbial loss and
recolonization in response to infection, recovering sifakas
exhibit remarkably consistent patterns, similar to initial
community assembly of the GMB in infants. This observation,
in particular, provides biological insight into the rules by
which the GMB recovers from the disease state. Fecal
transfaunation may prove effective in restoring a healthy
GMB in animals with specialized diets.},
Doi = {10.1080/16512235.2017.1335165},
Key = {fds345023}
}
@article{fds318203,
Author = {Davies, CS and Smyth, KN and Greene, LK and Walsh, DA and Mitchell, J and Clutton-Brock, T and Drea, CM},
Title = {Exceptional endocrine profiles characterise the meerkat:
sex, status, and reproductive patterns},
Journal = {Scientific Reports},
Volume = {6},
Pages = {35492},
Publisher = {The Author(s)},
Year = {2016},
Month = {October},
url = {http://dx.doi.org/10.1038/srep35492},
Abstract = {In vertebrates, reproductive endocrine concentrations are
strongly differentiated by sex, with androgen biases
typifying males and estrogen biases typifying females. These
sex differences can be reduced in female-dominant species;
however, even the most masculinised of females have less
testosterone (T) than do conspecific males. To test if
aggressively dominant, female meerkats (Suricata suricatta)
may be hormonally masculinised, we measured serum
androstenedione (A<sub>4</sub>), T and estradiol
(E<sub>2</sub>) in both sexes and social classes, during
both 'baseline' and reproductive events. Relative to
resident males, dominant females had greater A<sub>4</sub>,
equivalent T and greater E<sub>2</sub> concentrations.
Males, whose endocrine values did not vary by social status,
experienced increased T during reproductive forays, linking
T to sexual behaviour, but not social status. Moreover,
substantial E<sub>2</sub> concentrations in male meerkats
may facilitate their role as helpers. In females, dominance
status and pregnancy magnified the unusual concentrations of
measured sex steroids. Lastly, faecal androgen metabolites
replicated the findings derived from serum, highlighting the
female bias in total androgens. Female meerkats are thus
strongly hormonally masculinised, possibly via
A<sub>4</sub>'s bioavailability for conversion to T. These
raised androgen concentrations may explain female
aggressiveness in this species and give dominant breeders a
heritable mechanism for their daughters' competitive
edge.},
Doi = {10.1038/srep35492},
Key = {fds318203}
}
@article{fds331198,
Author = {Smyth, KN and Greene, LK and Clutton-Brock, T and Drea,
CM},
Title = {Androgens predict parasitism in female meerkats: a new
perspective on a classic trade-off.},
Journal = {Biology letters},
Volume = {12},
Number = {10},
Pages = {20160660},
Year = {2016},
Month = {October},
url = {http://dx.doi.org/10.1098/rsbl.2016.0660},
Abstract = {The immunocompetence handicap hypothesis posits that
androgens in males can be a 'double-edged sword', actively
promoting reproductive success, while also negatively
impacting health. Because there can be both substantial
androgen concentrations in females and significant
androgenic variation among them, particularly in species
portraying female social dominance over males or intense
female-female competition, androgens might also play a role
in mediating female health and fitness. We examined this
hypothesis in the meerkat (Suricata suricatta), a
cooperatively breeding, social carnivoran characterized by
aggressively mediated female social dominance and extreme
rank-related reproductive skew. Dominant females also have
greater androgen concentrations and harbour greater parasite
loads than their subordinate counterparts, but the
relationship between concurrent androgen concentrations and
parasite burdens is unknown. We found that a female's faecal
androgen concentrations reliably predicted her concurrent
state of endoparasitism irrespective of her social status:
parasite species richness and infection by Spirurida
nematodes, Oxynema suricattae, Pseudandrya suricattae and
coccidia were greater with greater androgen concentrations.
Based on gastrointestinal parasite burdens, females appear
to experience the same trade-off in the costs and benefits
of raised androgens as do the males of many species. This
trade-off presumably represents a health cost of sexual
selection operating in females.},
Doi = {10.1098/rsbl.2016.0660},
Key = {fds331198}
}
@article{fds321976,
Author = {Charpentier, MJE and Williams, CV and Drea, CM},
Title = {Erratum to: Inbreeding depression in ring-tailed lemurs
(Lemur catta): genetic diversity predicts parasitism,
immunocompetence, and survivorship(Conserv Genet, (2008), 9,
1605-1615, Doi:10.1007/s10592-007-9499-4)},
Journal = {Conservation Genetics},
Volume = {17},
Number = {3},
Pages = {751},
Publisher = {Springer Nature},
Year = {2016},
Month = {June},
url = {http://dx.doi.org/10.1007/s10592-015-0799-9},
Doi = {10.1007/s10592-015-0799-9},
Key = {fds321976}
}
@article{fds321977,
Author = {Greene, LK and Wallen, TW and Moresco, A and Goodwin, TE and Drea,
CM},
Title = {Reproductive endocrine patterns and volatile urinary
compounds of Arctictis binturong: discovering why bearcats
smell like popcorn.},
Journal = {Die Naturwissenschaften},
Volume = {103},
Number = {5-6},
Pages = {37},
Year = {2016},
Month = {June},
url = {http://dx.doi.org/10.1007/s00114-016-1361-4},
Abstract = {Members of the order Carnivora rely on urinary scent
signaling, particularly for communicating about reproductive
parameters. Here, we describe reproductive endocrine
patterns in relation to urinary olfactory cues in a
vulnerable and relatively unknown viverrid--the binturong
(Arctictis binturong). Female binturongs are larger than and
dominate males, and both sexes engage in glandular and
urinary scent marking. Using a large (n = 33), captive
population, we collected serum samples to measure
circulating sex steroids via enzyme immunoassay and urine
samples to assay volatile chemicals via gas
chromatography-mass spectrometry. Male binturongs had
expectedly greater androgen concentrations than did females
but, more unusually, had equal estrogen concentrations,
which may be linked to male deference. Males also expressed
a significantly richer array of volatile chemical compounds
than did females. A subset of these volatile chemicals
resisted decay at ambient temperatures, potentially
indicating their importance as long-lasting semiochemicals.
Among these compounds was 2-acetyl-1-pyrroline (2-AP), which
is typically produced at high temperatures by the Maillard
reaction and is likely to be responsible for the binturong's
characteristic popcorn aroma. 2-AP, the only compound
expressed by all of the subjects, was found in greater
abundance in males than females and was significantly and
positively related to circulating androstenedione
concentrations in both sexes. This unusual compound may have
a more significant role in mammalian semiochemistry than
previously appreciated. Based on these novel data, we
suggest that hormonal action and potentially complex
chemical reactions mediate communication of the binturong's
signature scent and convey information about sex and
reproductive state.},
Doi = {10.1007/s00114-016-1361-4},
Key = {fds321977}
}
@article{fds314362,
Author = {Greene, LK and Grogan, KE and Smyth, KN and Adams, CA and Klager, SA and Drea, CM},
Title = {Mix it and fix it: functions of composite olfactory signals
in ring-tailed lemurs},
Journal = {Royal Society Open Science},
Volume = {3},
Number = {4},
Pages = {160076},
Year = {2016},
Month = {April},
url = {http://hdl.handle.net/10161/11826 Duke open
access},
Abstract = {Animals communicating via scent often deposit composite
signals that incorporate odorants from multiple sources;
however, the function of mixing chemical signals remains
understudied. We tested both a ‘multiple-messages’ and a
‘fixative’ hypothesis of composite olfactory signalling,
which, respectively, posit that mixing scents functions to
increase information content or prolong signal longevity.
Our subjects—adult, male ring-tailed lemurs (Lemur
catta)—have a complex scent-marking repertoire, involving
volatile antebrachial (A) secretions, deposited pure or
after being mixed with a squalene-rich paste exuded from
brachial (B) glands. Using behavioural bioassays, we
examined recipient responses to odorants collected from
conspecific strangers. We concurrently presented pure A,
pure B and mixed A + B secretions, in fresh or decayed
conditions. Lemurs preferentially responded to mixed over
pure secretions, their interest increasing and shifting over
time, from sniffing and countermarking fresh mixtures, to
licking and countermarking decayed mixtures. Substituting
synthetic squalene (S)—a well-known fixative—for B
secretions did not replicate prior results: B secretions,
which contain additional chemicals that probably encode
salient information, were preferred over pure S. Whereas
support for the ‘multiple-messages’ hypothesis
underscores the unique contribution from each of an animal's
various secretions, support for the ‘fixative’
hypothesis highlights the synergistic benefits of composite
signals.},
Doi = {10.1098/rsos.160076},
Key = {fds314362}
}
@article{fds321978,
Author = {Grogan, KE and McGinnis, GJ and Sauther, ML and Cuozzo, FP and Drea,
CM},
Title = {Next-generation genotyping of hypervariable loci in many
individuals of a non-model species: technical and
theoretical implications.},
Journal = {BMC genomics},
Volume = {17},
Pages = {204},
Year = {2016},
Month = {March},
url = {http://dx.doi.org/10.1186/s12864-016-2503-y},
Abstract = {<h4>Background</h4>Across species, diversity at the Major
Histocompatibility Complex (MHC) is critical to disease
resistance and population health; however, use of MHC
diversity to quantify the genetic health of populations has
been hampered by the extreme variation found in MHC genes.
Next generation sequencing (NGS) technology generates
sufficient data to genotype even the most diverse species,
but workflows for distinguishing artifacts from alleles are
still under development. We used NGS to evaluate the MHC
diversity of over 300 captive and wild ring-tailed lemurs
(Lemur catta: Primates: Mammalia). We modified a published
workflow to address errors that arise from deep sequencing
individuals and tested for evidence of selection at the most
diverse MHC genes.<h4>Results</h4>In addition to evaluating
the accuracy of 454 Titanium and Ion Torrent PGM for
genotyping large populations at hypervariable genes, we
suggested modifications to improve current methods of allele
calling. Using these modifications, we genotyped 302 out of
319 individuals, obtaining an average sequencing depth of
over 1000 reads per amplicon. We identified 55 MHC-DRB
alleles, 51 of which were previously undescribed, and
provide the first sequences of five additional MHC genes:
DOA, DOB, DPA, DQA, and DRA. The additional five MHC genes
had one or two alleles each with little sequence variation;
however, the 55 MHC-DRB alleles showed a high dN/dS ratio
and trans-species polymorphism, indicating a history of
positive selection. Because each individual possessed 1-7
MHC-DRB alleles, we suggest that ring-tailed lemurs have
four, putatively functional, MHC-DRB copies.<h4>Conclusions</h4>In
the future, accurate genotyping methods for NGS data will be
critical to assessing genetic variation in non-model
species. We recommend that future NGS studies increase the
proportion of replicated samples, both within and across
platforms, particularly for hypervariable genes like the
MHC. Quantifying MHC diversity within non-model species is
the first step to assessing the relationship of genetic
diversity at functional loci to individual fitness and
population viability. Owing to MHC-DRB diversity and copy
number, ring-tailed lemurs may serve as an ideal model for
estimating the interaction between genetic diversity,
fitness, and environment, especially regarding endangered
species.},
Doi = {10.1186/s12864-016-2503-y},
Key = {fds321978}
}
@article{fds345054,
Author = {Grogan, KE and Boulet, M and Drea, CM},
Title = {Ring-tailed lemurs use olfactory signals to differentiate
the MHC quality of potential mates},
Journal = {AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY},
Volume = {159},
Pages = {162-162},
Publisher = {WILEY-BLACKWELL},
Year = {2016},
Month = {March},
Key = {fds345054}
}
@article{fds345055,
Author = {Smyth, KN and Davies, CS and Drea, CM},
Title = {The costs of being the boss: androgens and innate immunity
in a female-dominant species},
Journal = {INTEGRATIVE AND COMPARATIVE BIOLOGY},
Volume = {56},
Pages = {E206-E206},
Publisher = {OXFORD UNIV PRESS INC},
Year = {2016},
Month = {March},
Key = {fds345055}
}
@article{fds345056,
Author = {Grogan, KE and Sauther, ML and Cuozzo, FP and Drea,
CM},
Title = {The Influence of MHC on Reproductive Success in Wild
Ring-tailed Lemurs (Lemur catta)},
Journal = {INTEGRATIVE AND COMPARATIVE BIOLOGY},
Volume = {56},
Pages = {E80-E80},
Publisher = {OXFORD UNIV PRESS INC},
Year = {2016},
Month = {March},
Key = {fds345056}
}
@article{fds345057,
Author = {Davies, CS and Smyth, KN and Greene, LK and Drea,
CM},
Title = {Hormonal 'masculinization' in female meerkats (Suricata
suricatta)},
Journal = {INTEGRATIVE AND COMPARATIVE BIOLOGY},
Volume = {56},
Pages = {E50-E50},
Publisher = {OXFORD UNIV PRESS INC},
Year = {2016},
Month = {March},
Key = {fds345057}
}
@article{fds321979,
Author = {delBarco-Trillo, J and Greene, LK and Goncalves, IB and Fenkes, M and Wisse, JH and Drewe, JA and Manser, MB and Clutton-Brock, T and Drea,
CM},
Title = {Beyond aggression: Androgen-receptor blockade modulates
social interaction in wild meerkats.},
Journal = {Hormones and behavior},
Volume = {78},
Pages = {95-106},
Year = {2016},
Month = {February},
url = {http://dx.doi.org/10.1016/j.yhbeh.2015.11.001},
Abstract = {In male vertebrates, androgens are inextricably linked to
reproduction, social dominance, and aggression, often at the
cost of paternal investment or prosociality. Testosterone is
invoked to explain rank-related reproductive differences,
but its role within a status class, particularly among
subordinates, is underappreciated. Recent evidence,
especially for monogamous and cooperatively breeding
species, suggests broader androgenic mediation of adult
social interaction. We explored the actions of androgens in
subordinate, male members of a cooperatively breeding
species, the meerkat (Suricata suricatta). Although male
meerkats show no rank-related testosterone differences,
subordinate helpers rarely reproduce. We blocked androgen
receptors, in the field, by treating subordinate males with
the antiandrogen, flutamide. We monitored androgen
concentrations (via baseline serum and time-sequential fecal
sampling) and recorded behavior within their groups (via
focal observation). Relative to controls, flutamide-treated
animals initiated less and received more high-intensity
aggression (biting, threatening, feeding competition),
engaged in more prosocial behavior (social sniffing,
grooming, huddling), and less frequently initiated play or
assumed a 'dominant' role during play, revealing significant
androgenic effects across a broad range of social behavior.
By contrast, guarding or vigilance and measures of olfactory
and vocal communication in subordinate males appeared
unaffected by flutamide treatment. Thus, androgens in male
meerkat helpers are aligned with the traditional trade-off
between promoting reproductive and aggressive behavior at a
cost to affiliation. Our findings, based on rare endocrine
manipulation in wild mammals, show a more pervasive role for
androgens in adult social behavior than is often recognized,
with possible relevance for understanding tradeoffs in
cooperative systems.},
Doi = {10.1016/j.yhbeh.2015.11.001},
Key = {fds321979}
}
@article{fds321980,
Author = {Smyth, KN and Drea, CM},
Title = {Patterns of parasitism in the cooperatively breeding
meerkat: A cost of dominance for females},
Journal = {Behavioral Ecology},
Volume = {27},
Number = {1},
Pages = {148-157},
Publisher = {Oxford University Press (OUP)},
Year = {2016},
Month = {January},
url = {http://dx.doi.org/10.1093/beheco/arv132},
Abstract = {Within animal societies, demographic and social factors, as
well as the different reproductive efforts of group members,
may influence individual patterns of reproductive success
and parasitism. In mammals, such relationships have been
studied primarily in male-dominant species. To better
understand these linkages in other social systems, we
studied a female-dominant cooperative breeder, the meerkat
(Suricata suricatta). This species is characterized by
intense intrasexual competition and extreme reproductive
skew in both sexes. Within adults, we examined
heterogeneities in infection by 6 species of endoparasites
in relation to host factors (e.g., weight, age, social
status, sex, and group size). We explored potential
trade-offs between reproduction and parasitism in dominant
and subordinate animals of both sexes. Whereas weight and
age were predictive of a few parasite taxa, social status or
sex predicted parasite species richness and patterns of
infection for the majority of parasites examined. Moreover,
a significant interaction between sex and status for 2
nematode taxa revealed that dominant females were the most
at risk of infection. Lastly, a positive relationship
between group size and parasitism was evident in females
only. In sum, compared with subordinates, dominant meerkats
may experience increased exposure to directly transmitted
parasites. Coupled with hormone-mediated immunosuppression,
the increased susceptibility of dominant females may reflect
energy allocation for preferentially maintaining dominance
and breeding status over parasite defense. In species in
which female intrasexual competition is intense, this
trade-off between reproduction and health may be more
pronounced in females than in males.},
Doi = {10.1093/beheco/arv132},
Key = {fds321980}
}
@article{fds240142,
Author = {Petty, JMA and Drea, CM},
Title = {Female rule in lemurs is ancestral and hormonally
mediated.},
Journal = {Scientific reports},
Volume = {5},
Pages = {9631},
Year = {2015},
Month = {May},
url = {http://dx.doi.org/10.1038/srep09631},
Abstract = {Female social dominance (FSD) over males is unusual in
mammals, yet characterizes most Malagasy lemurs, which
represent almost 30% of all primates. Despite its prevalence
in this suborder, both the evolutionary trajectory and
proximate mechanism of FSD remain unclear. Potentially
associated with FSD is a suite of behavioural, physiological
and morphological traits in females that implicates (as a
putative mechanism) 'masculinization' via androgen exposure;
however, relative to conspecific males, female lemurs
curiously show little evidence of raised androgen
concentrations. By observing mixed-sex pairs of related
Eulemur species, we identified two key study groups--one
comprised of species expressing FSD and increased female
scent marking, the other comprised of species (from a
recently evolved clade) showing equal status between the
sexes and the more traditional pattern of sexually dimorphic
behaviour. Comparing females from these two groups, we show
that FSD is associated with more masculine androgen
profiles. Based on the widespread prevalence of male-like
features in female lemurs and a current phylogeny, we
suggest that relaxation of hormonally mediated FSD emerged
only recently and that female masculinization may be the
ancestral lemur condition, an idea that could revolutionize
our understanding of the ancient socioecology and evolution
of primate social systems.},
Doi = {10.1038/srep09631},
Key = {fds240142}
}
@article{fds240143,
Author = {Crawford, JC and Drea, CM},
Title = {Baby on board: olfactory cues indicate pregnancy and fetal
sex in a non-human primate},
Journal = {Biology Letters},
Volume = {11},
Number = {2},
Pages = {20140831},
Year = {2015},
Month = {February},
ISSN = {1744-9561},
url = {http://hdl.handle.net/10161/9493 Duke open
access},
Abstract = {Jeremy Chase Crawford1,2,3,4 and Christine M.
Drea4,5⇑1National Evolutionary Synthesis Center, Durham,
NC, USA2Department of Integrative Biology, University of
California, Berkeley, CA, USA3Museum of Vertebrate Zoology,
University of California, Berkeley, CA, USA4Department of
Evolutionary Anthropology, Duke University, Durham, NC,
USA5Department of Biology, Duke University, Durham, NC,
USAe-mail: cdrea{at}duke.eduAbstract Olfactory cues play an
integral, albeit underappreciated, role in mediating
vertebrate social and reproductive behaviour. These cues
fluctuate with the signaller's hormonal condition,
coincident with and informative about relevant aspects of
its reproductive state, such as pubertal onset, change in
season and, in females, timing of ovulation. Although
pregnancy dramatically alters a female's endocrine
profiles, which can be further influenced by fetal sex, the
relationship between gestation and olfactory cues is poorly
understood. We therefore examined the effects of pregnancy
and fetal sex on volatile genital secretions in the
ring-tailed lemur (Lemur catta), a strepsirrhine primate
possessing complex olfactory mechanisms of reproductive
signalling. While pregnant, dams altered and dampened their
expression of volatile chemicals, with compound richness
being particularly reduced in dams bearing sons. These
changes were comparable in magnitude with other, published
chemical differences among lemurs that are salient to
conspecifics. Such olfactory ‘signatures’ of pregnancy
may help guide social interactions, potentially promoting
mother–infant recognition, reducing intragroup conflict or
counteracting behavioural mechanisms of paternity confusion;
cues that also advertise fetal sex may additionally
facilitate differential sex allocation. olfactory
communicationreproductive signalgestationsex
allocationhormonechemosignalReceived October 27,
2014.Accepted January 20, 2015.© 2015 The Author(s)
Published by the Royal Society. All rights
reserved.},
Doi = {10.1098/rsbl.2014.0831},
Key = {fds240143}
}
@article{fds240149,
Author = {Drea, CM},
Title = {D'scent of man: a comparative survey of primate
chemosignaling in relation to sex.},
Journal = {Hormones and behavior},
Volume = {68},
Pages = {117-133},
Year = {2015},
Month = {February},
ISSN = {0018-506X},
url = {http://dx.doi.org/10.1016/j.yhbeh.2014.08.001},
Abstract = {This article is part of a Special Issue (Chemosignals and
Reproduction). As highly visual animals, primates, in
general, and Old World species (including humans), in
particular, are not immediately recognized for reliance in
their daily interactions on olfactory communication.
Nevertheless, views on primate olfactory acuity and the
pervasiveness of their scent signaling are changing, with
increased appreciation for the important role of body odors
in primate social and sexual behavior. All major taxonomic
groups, from lemurs to humans, are endowed with
scent-producing organs, and either deposit or exude a wealth
of volatile compounds, many of which are known
semiochemicals. This review takes a comparative perspective
to illustrate the reproductive context of primate signaling,
the relevant information content of their signals, the
sexually differentiated investigative responses generated,
and the behavioral or physiological consequences of message
transmission to both signaler and receiver. Throughout,
humans are placed alongside their relatives to illustrate
the evolutionary continuum in the sexual selection of
primate chemosignals. This ever-growing body of evidence
points to a critical role of scent in guiding the social
behavior and reproductive function throughout the primate
order.},
Doi = {10.1016/j.yhbeh.2014.08.001},
Key = {fds240149}
}
@article{fds240146,
Author = {delBarco-Trillo, J and Drea, CM},
Title = {Socioecological and phylogenetic patterns in the chemical
signals of strepsirrhine primates},
Journal = {Animal Behaviour},
Volume = {97},
Pages = {249-253},
Year = {2014},
Month = {November},
ISSN = {0003-3472},
url = {http://dx.doi.org/10.1016/j.anbehav.2014.07.009},
Abstract = {Our understanding of chemical signals in mammals derives
principally from studies in which researchers examine signal
structure or function within a single species. Despite the
unique information to be gained from applying comparable
methods across multiple species, comparative studies of
chemical signals are extremely limited. Here, we review the
available literature on the evolution of chemosignals in
male and female strepsirrhine primates (galagos, lorises and
lemurs), all of which rely heavily on chemical
communication. We draw from a few case studies, but focus
our review on two comparative studies. In one, researchers
examined the volatile chemical composition of urinary
signals across 12 species representing most families within
Strepsirrhini, including six 'urine-marking' species and six
glandular or 'nonurine-marking' species. In the other,
researchers examined the volatile chemical composition of
glandular signals in eight Eulemur species differing in
social or dominance structure. We highlight five findings.
(1) Regardless of the scent source, chemical profiles differ
substantially between species, providing reliable species
'scent signatures'. None the less, (2) urine markers express
more compounds and have more distinguishable species scent
signatures in their urine than do nonurine markers,
suggesting specialization of function. Within Eulemur (3)
chemical richness is greater in multimale-multifemale
species than in pair-bonded species. Moreover, (4) whereas
chemical richness of male signals is greater in sexually
codominant species, chemical richness of female signals is
greater in female-dominant species. Together, the findings
from both comparative studies, coupled with case studies,
suggest that signal richness is linked to some aspect of the
focal species' socioecology. Lastly, (5) regardless of the
scent source, strepsirrhine chemosignals evolve gradually
over time, but at fast rates and homogeneously within
different lineages. Comparative studies reveal patterns that
cannot be detected from the single-species approach and are
therefore critical for providing new insight into the
function and evolution of olfactory signals.},
Doi = {10.1016/j.anbehav.2014.07.009},
Key = {fds240146}
}
@article{fds240152,
Author = {Kulahci, IG and Drea, CM and Rubenstein, DI and Ghazanfar,
AA},
Title = {Individual recognition through olfactory-auditory matching
in lemurs.},
Journal = {Proceedings. Biological sciences},
Volume = {281},
Number = {1784},
Pages = {20140071},
Year = {2014},
Month = {June},
ISSN = {0962-8452},
url = {http://dx.doi.org/10.1098/rspb.2014.0071},
Abstract = {Individual recognition can be facilitated by creating
representations of familiar individuals, whereby information
from signals in multiple sensory modalities become linked.
Many vertebrate species use auditory-visual matching to
recognize familiar conspecifics and heterospecifics, but we
currently do not know whether representations of familiar
individuals incorporate information from other modalities.
Ring-tailed lemurs (Lemur catta) are highly visual, but also
communicate via scents and vocalizations. To investigate the
role of olfactory signals in multisensory recognition, we
tested whether lemurs can recognize familiar individuals
through matching scents and vocalizations. We presented
lemurs with female scents that were paired with the contact
call either of the female whose scent was presented or of
another familiar female from the same social group. When the
scent and the vocalization came from the same individual
versus from different individuals, females showed greater
interest in the scents, and males showed greater interest in
both the scents and the vocalizations, suggesting that
lemurs can recognize familiar females via olfactory-auditory
matching. Because identity signals in lemur scents and
vocalizations are produced by different effectors and often
encountered at different times (uncoupled in space and
time), this matching suggests lemurs form multisensory
representations through a newly recognized sensory
integration underlying individual recognition.},
Doi = {10.1098/rspb.2014.0071},
Key = {fds240152}
}
@article{fds240153,
Author = {Grogan, KE and Sauther, ML and Cuozzo, FP and Drea,
CM},
Title = {The impact of genetic variation at the Major
Histocompatibility Complex in captive and wild ring-tailed
lemurs (Lemur catta)},
Journal = {AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY},
Volume = {153},
Pages = {131-131},
Publisher = {WILEY-BLACKWELL},
Year = {2014},
Month = {March},
ISSN = {0002-9483},
url = {http://gateway.webofknowledge.com/gateway/Gateway.cgi?GWVersion=2&SrcApp=PARTNER_APP&SrcAuth=LinksAMR&KeyUT=WOS:000331225100300&DestLinkType=FullRecord&DestApp=ALL_WOS&UsrCustomerID=47d3190e77e5a3a53558812f597b0b92},
Key = {fds240153}
}
@article{fds240154,
Author = {Drea, CM},
Title = {Reassessing Bateman: Sexual selection in strepsirrhine
primates},
Journal = {AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY},
Volume = {153},
Pages = {108-108},
Publisher = {WILEY-BLACKWELL},
Year = {2014},
Month = {March},
ISSN = {0002-9483},
url = {http://gateway.webofknowledge.com/gateway/Gateway.cgi?GWVersion=2&SrcApp=PARTNER_APP&SrcAuth=LinksAMR&KeyUT=WOS:000331225100198&DestLinkType=FullRecord&DestApp=ALL_WOS&UsrCustomerID=47d3190e77e5a3a53558812f597b0b92},
Key = {fds240154}
}
@article{fds240155,
Author = {Greene, LK and Drea, CM},
Title = {Love is in the air: Sociality and pair bondedness influence
sifaka reproductive signalling},
Journal = {Animal Behaviour},
Volume = {88},
Pages = {147-156},
Publisher = {Elsevier BV},
Year = {2014},
Month = {February},
ISSN = {0003-3472},
url = {http://hdl.handle.net/10161/8368 Duke open
access},
Abstract = {Social complexity, often estimated by group size, is seen as
driving the complexity of vocal signals, but its relation to
olfactory signals, which arguably arose to function in
nonsocial realms, remains underappreciated. That olfactory
signals also may mediate within-group interaction, vary with
social complexity and promote social cohesion underscores a
potentially crucial link with sociality. To examine that
link, we integrated chemical and behavioural analyses to ask
whether olfactory signals facilitate reproductive
coordination in a strepsirrhine primate, the Coquerel's
sifaka, Propithecus coquereli. Belonging to a clade
comprising primarily solitary, nocturnal species, the
diurnal, group-living sifaka represents an interesting test
case. Convergent with diurnal, group-living lemurids,
sifakas expressed chemically rich scent signals, consistent
with the social complexity hypothesis for communication.
These signals minimally encoded the sex of the signaller and
varied with female reproductive state. Likewise, sex and
female fertility were reflected in within-group scent
investigation, scent marking and overmarking. We further
asked whether, within breeding pairs, the stability or
quality of the pair's bond influences the composition of
glandular signals and patterns of investigatory or
scent-marking behaviour. Indeed, reproductively successful
pairs tended to show greater similarity in their scent
signals than did reproductively unsuccessful pairs,
potentially through chemical convergence. Moreover, scent
marking was temporally coordinated within breeding pairs and
was influenced by past reproductive success. That olfactory
signalling reflects social bondedness or reproductive
history lends support to recent suggestions that the quality
of relationships may be a more valuable proxy than group
size for estimating social complexity. We suggest that
olfactory signalling in sifakas is more complex than
previously recognized and, as in other socially integrated
species, can be a crucial mechanism for promoting group
cohesion and maintaining social bonds. Thus, the evolution
of sociality may well be reflected in the complexity of
olfactory signalling.},
Doi = {10.1016/j.anbehav.2013.11.019},
Key = {fds240155}
}
@article{fds240150,
Author = {Leclaire, S and Nielsen, JF and Drea, CM},
Title = {Bacterial communities in meerkat anal scent secretions vary
with host sex, age, and group membership},
Journal = {Behavioral Ecology},
Volume = {25},
Number = {4},
Pages = {996-1004},
Publisher = {Oxford University Press (OUP)},
Year = {2014},
Month = {January},
ISSN = {1045-2249},
url = {http://dx.doi.org/10.1093/beheco/aru074},
Abstract = {The contribution of bacterial fermentation to the production
of vertebrate scent signals has long been suspected, but
there is still relatively little information about the
factors driving variation in microbial composition in animal
scent secretions. Our study subject, the meerkat (Suricata
suricatta), is a social mongoose that lives in territorial,
family groups and relies heavily on scent for social
communication. Unusually in mammalian research, extensive
life-history data exist for multiple groups inhabiting the
same ecosystem, allowing for a study of both individual
variation and group differences in the host's microbial
communities. Using a culture-independent sampling technique,
we explored the relationship between a signaler's sex,
age/dominance, genotype or group membership, and the
microbiota of its anal scent secretions. We found
differences in the microbiota of males and females, but only
after the animals had reached sexual maturity. Although
bacterial communities in meerkat scent secretions were not
more similar between kin than between nonkin, they were more
similar between members of the same group than between
members of different groups. Collectively, these results are
consistent with a potential role for reproductive hormones
in determining a host's bacterial assemblages, as well as an
influence of sociality (such as intragroup allo-marking
behavior) and/or microhabitat in the acquisition of
bacterial assemblages. This study provides a key starting
point for understanding the role of microbes in the
variation of scent composition in mammals. © 2014 The
Author.},
Doi = {10.1093/beheco/aru074},
Key = {fds240150}
}
@article{fds240151,
Author = {Cunha, GR and Risbridger, G and Wang, H and Place, NJ and Grumbach, M and Cunha, TJ and Weldele, M and Conley, AJ and Barcellos, D and Agarwal, S and Bhargava, A and Drea, C and Hammond, GL and Siiteri, P and Coscia, EM and McPhaul, MJ and Baskin, LS and Glickman, SE},
Title = {Development of the external genitalia: perspectives from the
spotted hyena (Crocuta crocuta).},
Journal = {Differentiation; research in biological diversity},
Volume = {87},
Number = {1-2},
Pages = {4-22},
Year = {2014},
Month = {January},
ISSN = {0301-4681},
url = {http://dx.doi.org/10.1016/j.diff.2013.12.003},
Abstract = {This review/research paper summarizes data on development of
the external genitalia of the spotted hyena, a fascinating
mammal noted for extreme masculinization of the female
external genitalia. The female spotted hyena is the only
extant mammal that mates and gives birth through a pendulous
penis-like clitoris. Our studies indicate that early
formation of the phallus in both males and females is
independent of androgens; indeed the phallus forms before
the fetal testes or ovaries are capable of synthesizing
androgens. Likewise, pre- and postnatal growth in length of
the penis and clitoris is minimally affected by "androgen
status". Nonetheless, several internal morphologies, as well
as external surface features of the phallus, are
androgen-dependent and thus account for dimorphism between
the penis and clitoris. Finally, estrogens play a critical
role in penile and clitoral development, specifying the
position of the urethral orifice, determining elasticity of
the urethral meatus, and facilitating epithelial-epithelial
fusion events required for proper formation of the distal
urethra/urogenital sinus and prepuce. Accordingly, prenatal
inhibition of estrogen synthesis via administration of
letrozole (an aromatase inhibitor) leads to malformations of
the glans as well as the prepuce (hypospadias). The effects
of prenatal androgens, anti-androgens and impaired estrogen
synthesis correlated with the tissue expression of androgen
and estrogen receptors.},
Doi = {10.1016/j.diff.2013.12.003},
Key = {fds240151}
}
@article{fds240161,
Author = {Drea, CM and Boulet, M and Delbarco-Trillo, J and Greene, LK and Sacha,
CR and Goodwin, TE and Dubay, GR},
Title = {The "secret" in secretions: methodological considerations in
deciphering primate olfactory communication.},
Journal = {American journal of primatology},
Volume = {75},
Number = {7},
Pages = {621-642},
Year = {2013},
Month = {July},
ISSN = {0275-2565},
url = {http://www.ncbi.nlm.nih.gov/pubmed/23526595},
Abstract = {Olfactory communication in primates is gaining recognition;
however, studies on the production and perception of primate
scent signals are still scant. In general, there are five
tasks to be accomplished when deciphering the chemical
signals contained in excretions and secretions: (1)
obtaining the appropriate samples; (2) extracting the target
organic compounds from the biological matrix; (3) separating
the extracted compounds from one another (by gas
chromatography, GC or liquid chromatography, LC); (4)
identifying the compounds (by mass spectrometry, MS and
associated procedures); and (5) revealing biologically
meaningful patterns in the data. Ultimately, because some of
the compounds identified in odorants may not be relevant,
associated steps in understanding signal function involve
verifying the perception or biological activity of putative
semiochemicals via (6) behavioral bioassays or (7) receptor
response studies. This review will focus on the chemical
analyses and behavioral bioassays of volatile, primate scent
signals. Throughout, we highlight the potential pitfalls of
working with highly complex, chemical matrices and suggest
ways for minimizing problems. A recurring theme in this
review is that multiple approaches and instrumentation are
required to characterize the full range of information
contained in the complex mixtures that typify primate or,
indeed, many vertebrate olfactory cues. Only by integrating
studies of signal production with those verifying signal
perception will we better understand the function of
olfactory communication.},
Doi = {10.1002/ajp.22143},
Key = {fds240161}
}
@article{fds240192,
Author = {Delbarco-Trillo, J and Harelimana, IH and Goodwin, TE and Drea,
CM},
Title = {Chemical differences between voided and bladder urine in the
aye-aye (Daubentonia madagascariensis): implications for
olfactory communication studies.},
Journal = {American journal of primatology},
Volume = {75},
Number = {7},
Pages = {695-702},
Year = {2013},
Month = {July},
ISSN = {0275-2565},
url = {http://www.ncbi.nlm.nih.gov/pubmed/23027610},
Abstract = {Urine serves a communicative function in many mammalian
species. In some species, the signaling function of urine
can be enhanced by the addition of chemical compounds from
glands along the distal portion of the urogenital tract.
Although urine marking is the main mode of chemical
communication in many primate species, there has been no
study of the contribution of urogenital secretions to the
chemical complexity of primate urine. Here, we compared the
chemical composition of bladder urine versus voided urine in
the aye-aye, Daubentonia madagascariensis, a strepsirrhine
primate that relies on urine in intraspecific communication.
Both types of urine, collected from each of 11 aye-ayes
representing both sexes of varying adult ages, underwent
headspace analysis via gas chromatography and mass
spectrometry. Although the average number of compounds was
similar in bladder and voided urine, 17% of the compounds
detected occurred exclusively in voided urine (but only in a
subset of individuals). An overall measure of chemical
complexity (using a nonmetric multidimensional scaling
analysis) showed that both types of urine were chemically
different at the individual level. There was no apparent sex
or age differences in the chemical components found in
aye-aye urine. Nonetheless, the individual dissimilarities
between bladder urine and voided urine indicate chemical
contributions from structures along the urogenital tract and
offer further support for the relevance of urinary
communication in the aye-aye.},
Doi = {10.1002/ajp.22083},
Key = {fds240192}
}
@article{fds286472,
Author = {Charpentier, MJE and Mboumba, S and Ditsoga, C and Drea,
CM},
Title = {Nasopalatine ducts and flehmen behavior in the mandrill:
reevaluating olfactory communication in Old World
primates.},
Journal = {American journal of primatology},
Volume = {75},
Number = {7},
Pages = {703-714},
Year = {2013},
Month = {July},
url = {http://www.ncbi.nlm.nih.gov/pubmed/23526642},
Abstract = {Compared to other modes of communication, chemical signaling
between conspecifics generally has been overlooked in Old
World primates, despite the presence in this group of
secretory glands and scent-marking behavior, as well as the
confirmed production and perception of olfactory signals. In
other mammalian species, flehmen is a behavior thought to
transport primarily nonvolatile, aqueous-soluble odorants
via specialized ducts to the vomeronasal organ (VNO). By
contrast, Old World primates are traditionally thought to
lack a functional VNO, relying instead on the main olfactory
system to process volatile odorants from their environment.
Here, in the mandrill (Mandrillus sphinx), we document
unusual morphological and behavioral traits that typically
are associated with the uptake of conspecific chemical cues
for processing by an accessory olfactory system. Notably, we
confirmed that both sexes possess open nasopalatine ducts
and, in response to the presentation of conspecific
odorants, we found that both sexes showed stereotyped
behavior consistent with the flehmen response. If, as in
other species, flehmen in the mandrill serves to mediate
social or reproductive information, we expected its
occurrence to vary with characteristics of either the
signaler or receiver. Flehmen, particularly in a given male,
occurred most often in response to odorants derived from
male, as opposed to female, conspecifics. Moreover, odorants
derived during the breeding season elicited more flehmen
responses than did odorants collected during the birthing
season. Lastly, odorants from reproductively cycling females
also elicited more responses than did odorants from
contracepted females. Although confirming a link between the
nasopalatine ducts, flehmen behavior, and olfactory
processing in mandrills would require further study, our
observations provide new information to suggest anatomical
variability within Old World primates, calling further
attention to the underappreciated role of chemical
communication in this lineage.},
Doi = {10.1002/ajp.22146},
Key = {fds286472}
}
@article{fds240156,
Author = {Charpentier, MJE and Drea, CM},
Title = {Victims of infanticide and conspecific bite wounding in a
female-dominant primate: a long-term study.},
Journal = {PloS one},
Volume = {8},
Number = {12},
Pages = {e82830},
Year = {2013},
Month = {January},
url = {http://www.ncbi.nlm.nih.gov/pubmed/24367560},
Abstract = {The aggression animals receive from conspecifics varies
between individuals across their lifetime. As poignantly
evidenced by infanticide, for example, aggression can have
dramatic fitness consequences. Nevertheless, we understand
little about the sources of variation in received
aggression, particularly in females. Using a female-dominant
species renowned for aggressivity in both sexes, we tested
for potential social, demographic, and genetic patterns in
the frequency with which animals were wounded by
conspecifics. Our study included 243 captive, ring-tailed
lemurs (Lemur catta), followed from infancy to adulthood
over a 35-year time span. We extracted injury, social, and
life-history information from colony records and calculated
neutral heterozygosity for a subset of animals, as an
estimate of genetic diversity. Focusing on victims rather
than aggressors, we used General Linear Models to explain
bite-wound patterns at different life stages. In infancy,
maternal age best predicted wounds received, as infants born
to young mothers were the most frequent infanticide victims.
In adulthood, sex best predicted wounds received, as males
were three times more likely than females to be seriously
injured. No relation emerged between wounds received and the
other variables studied. Beyond the generally expected costs
of adult male intrasexual aggression, we suggest possible
additive costs associated with female-dominant societies -
those suffered by young mothers engaged in aggressive
disputes and those suffered by adult males aggressively
targeted by both sexes. We propose that infanticide in
lemurs may be a costly by-product of aggressively mediated,
female social dominance. Accordingly, the benefits of female
behavioral 'masculinization' accrued to females through
priority of access to resources, may be partially offset by
early costs in reproductive success. Understanding the
factors that influence lifetime patterns of conspecific
wounding is critical to evaluating the fitness costs
associated with social living; however, these costs may vary
substantially between societies.},
Doi = {10.1371/journal.pone.0082830},
Key = {fds240156}
}
@article{fds220544,
Author = {Cunha, G.R. and Risbridger, G. and Wang, H. and Place, N.J. and Wilson, J. and Grumbach, M. and Siiteri, P. and Cunha, T.J. and Conley, A.J. and Barcellos, D. and Agarwal, S. and Bhargava, A. and Drea, C.M. and Hammond, G. and Weldele, M. and Baskin, L.S. and Glickman, S.},
Title = {Development of the external genitalia: Perspectives from the
spotted hyena},
Journal = {Differentiation},
Year = {2013},
Key = {fds220544}
}
@article{fds240193,
Author = {delBarco-Trillo, J and Sacha, CR and Dubay, GR and Drea,
CM},
Title = {Eulemur, me lemur: the evolution of scent-signal complexity
in a primate clade.},
Journal = {Philosophical transactions of the Royal Society of London.
Series B, Biological sciences},
Volume = {367},
Number = {1597},
Pages = {1909-1922},
Year = {2012},
Month = {July},
url = {http://www.ncbi.nlm.nih.gov/pubmed/22641829},
Abstract = {Signal complexity has been linked to social complexity in
vocal, but not chemical, communication. To address this gap,
we examined the chemical complexity of male and female
glandular secretions in eight species of Eulemur. In this
diverse clade of macrosmatic primates, species differ by
social or mating system and dominance structure. We applied
principal component and linear discriminate analyses to data
obtained by gas chromatography/mass spectrometry. Beyond the
significant effects on chemical signals of gland type, sex,
season and species, we found effects of social variables and
phylogeny. Notably, female odours were more chemically
complex in multimale-multifemale species than pair-bonded
species, whereas male odours were more chemically complex in
codominant species than female-dominant species. Also, the
traditional sexual dimorphism, whereby male signal
complexity exceeds that of females, was present in
codominant species, but reversed in female-dominant species.
Lastly, a positive relationship between the species'
pairwise chemical distances and their pairwise phylogenetic
distances supported a gradual, but relatively fast mode of
signal evolution. We suggest that the comparative method can
be a powerful tool in olfactory research, revealing species
differences relevant to the understanding of current signal
utility and evolutionary processes. In particular, social
complexity in lemurs may have selected for olfactory
complexity.},
Doi = {10.1098/rstb.2011.0225},
Key = {fds240193}
}
@article{fds240194,
Author = {MacLean, EL and Matthews, LJ and Hare, BA and Nunn, CL and Anderson, RC and Aureli, F and Brannon, EM and Call, J and Drea, CM and Emery, NJ and Haun,
DBM and Herrmann, E and Jacobs, LF and Platt, ML and Rosati, AG and Sandel,
AA and Schroepfer, KK and Seed, AM and Tan, J and van Schaik, CP and Wobber, V},
Title = {How does cognition evolve? Phylogenetic comparative
psychology.},
Journal = {Anim Cogn},
Volume = {15},
Number = {2},
Pages = {223-238},
Year = {2012},
Month = {March},
url = {http://www.ncbi.nlm.nih.gov/pubmed/21927850},
Abstract = {Now more than ever animal studies have the potential to test
hypotheses regarding how cognition evolves. Comparative
psychologists have developed new techniques to probe the
cognitive mechanisms underlying animal behavior, and they
have become increasingly skillful at adapting methodologies
to test multiple species. Meanwhile, evolutionary biologists
have generated quantitative approaches to investigate the
phylogenetic distribution and function of phenotypic traits,
including cognition. In particular, phylogenetic methods can
quantitatively (1) test whether specific cognitive abilities
are correlated with life history (e.g., lifespan),
morphology (e.g., brain size), or socio-ecological variables
(e.g., social system), (2) measure how strongly phylogenetic
relatedness predicts the distribution of cognitive skills
across species, and (3) estimate the ancestral state of a
given cognitive trait using measures of cognitive
performance from extant species. Phylogenetic methods can
also be used to guide the selection of species comparisons
that offer the strongest tests of a priori predictions of
cognitive evolutionary hypotheses (i.e., phylogenetic
targeting). Here, we explain how an integration of
comparative psychology and evolutionary biology will answer
a host of questions regarding the phylogenetic distribution
and history of cognitive traits, as well as the evolutionary
processes that drove their evolution.},
Doi = {10.1007/s10071-011-0448-8},
Key = {fds240194}
}
@article{fds240195,
Author = {Hammond, GL and Miguel-Queralt, S and Yalcinkaya, TM and Underhill,
C and Place, NJ and Glickman, SE and Drea, CM and Wagner, AP and Siiteri,
PK},
Title = {Phylogenetic comparisons implicate sex hormone-binding
globulin in "masculinization" of the female spotted hyena
(Crocuta crocuta).},
Journal = {Endocrinology},
Volume = {153},
Number = {3},
Pages = {1435-1443},
Year = {2012},
Month = {March},
url = {http://www.ncbi.nlm.nih.gov/pubmed/22253421},
Abstract = {Exposures to sex steroids during fetal development are
thought to contribute to the unique urogenital anatomy and
social dominance of the female spotted hyena: overt
phenotypes not shared by other hyenids (i.e. striped hyena,
brown hyena, and aardwolf). Because both androgens and
estrogens influence development of genitalia and behavior,
and because plasma SHBG regulates their access to tissues,
we compared the Shbg gene sequences, structures, and
steroid-binding properties in the four extant hyenids. We
found the hyenid Shbg genes (>95% identical) and mature
protein sequences (98% identical) are highly conserved. As
in other mammals, the hyenid SHBG all bind
5α-dihydrotestosterone with high affinity (K(d) = 0.62-1.47
nm), but they also bind estrone and dehydroepiandrosterone
with similarly high affinity, and this unusual property was
attributed to specific amino acids within their SHBG
steroid-binding sites. Phylogenetic comparisons also
indicated that the spotted hyena SHBG precursor uniquely
lacks two leucine residues and has a L15W substitution
within its secretion signal polypeptide, the reduced size
and hydrophobicity of which markedly decreases the
production of SHBG and may therefore explain why serum SHBG
concentrations in male and female spotted hyenas are
approximately five times lower than in other hyenids. This
is important because low plasma SHBG concentrations in
spotted hyenas will increase exposure to biologically active
androgens and estrogen as well as to their precursors
(dehydroepiandrosterone and estrone), which may contribute
to the masculinized external genitalia of female spotted
hyenas and to female social dominance over
males.},
Doi = {10.1210/en.2011-1837},
Key = {fds240195}
}
@article{fds240196,
Author = {Rushmore, J and Leonhardt, SD and Drea, CM},
Title = {Sight or scent: lemur sensory reliance in detecting food
quality varies with feeding ecology.},
Journal = {PloS one},
Volume = {7},
Number = {8},
Pages = {e41558},
Year = {2012},
Month = {January},
url = {http://www.ncbi.nlm.nih.gov/pubmed/22870229},
Abstract = {Visual and olfactory cues provide important information to
foragers, yet we know little about species differences in
sensory reliance during food selection. In a series of
experimental foraging studies, we examined the relative
reliance on vision versus olfaction in three diurnal,
primate species with diverse feeding ecologies, including
folivorous Coquerel's sifakas (Propithecus coquereli),
frugivorous ruffed lemurs (Varecia variegata spp), and
generalist ring-tailed lemurs (Lemur catta). We used animals
with known color-vision status and foods for which different
maturation stages (and hence quality) produce distinct
visual and olfactory cues (the latter determined
chemically). We first showed that lemurs preferentially
selected high-quality foods over low-quality foods when
visual and olfactory cues were simultaneously available for
both food types. Next, using a novel apparatus in a series
of discrimination trials, we either manipulated food quality
(while holding sensory cues constant) or manipulated sensory
cues (while holding food quality constant). Among our study
subjects that showed relatively strong preferences for
high-quality foods, folivores required both sensory cues
combined to reliably identify their preferred foods, whereas
generalists could identify their preferred foods using
either cue alone, and frugivores could identify their
preferred foods using olfactory, but not visual, cues alone.
Moreover, when only high-quality foods were available,
folivores and generalists used visual rather than olfactory
cues to select food, whereas frugivores used both cue types
equally. Lastly, individuals in all three of the study
species predominantly relied on sight when choosing between
low-quality foods, but species differed in the strength of
their sensory biases. Our results generally emphasize visual
over olfactory reliance in foraging lemurs, but we suggest
that the relative sensory reliance of animals may vary with
their feeding ecology.},
Doi = {10.1371/journal.pone.0041558},
Key = {fds240196}
}
@article{fds240191,
Author = {Charpentier, MJE and Ditsoga, C and Mboumba, S and Drea,
CM},
Title = {Nasopalatine ducts and flehmen behavior in the mandrill
(Mandrillus sphinx): Reevaluating olfactory communication in
primates.},
Journal = {American Journal of Primatology},
Volume = {75},
Number = {7},
Pages = {703-714},
Year = {2012},
url = {http://dx.doi.org/10.1002/ajp.22146},
Abstract = {Compared to other modes of communication, chemical signaling
generally has been overlooked in Old World primates, despite
the presence in this group of secretory glands and
scent-marking behavior, as well as the confirmed production
and perception of conspecific olfactory signals. In other
mammalian species, flehmen is a behavior thought to
transport nonvolatile, aqueous-soluble odorants via
specialized ducts to the vomeronasal organ (VNO). By
contrast, Old World primates are traditionally thought to
lack a functional VNO, relying only on the main olfactory
system to process volatile odorants from their environment.
Here, in the mandrill (Mandrillus sphinx), we document
unusual morphological and behavioral traits that typically
are associated with the uptake of conspecific chemical cues
for processing by an accessory olfactory system. Notably,
both sexes possess open nasopalatine ducts and, in response
to the presentation of conspecific odorants, show
stereotyped behavior consistent with the flehmen response.
Flehmen occurred more frequently in response to odorants
derived from male, as opposed to female, conspecifics and to
odorants derived during the breeding season than the
birthing season, suggesting a possible role in mediating
social or reproductive information. Although confirming a
link between the nasopalatine ducts, flehmen behavior, and
olfactory processing in mandrills would require further
study, our observations provide new information to suggest
anatomical variability within Old World primates, calling
further attention to the underappreciated role of chemical
communication in this lineage.},
Doi = {10.1002/ajp.22146},
Key = {fds240191}
}
@article{fds240197,
Author = {Drea, CM},
Title = {Endocrine correlates of pregnancy in the ring-tailed lemur
(Lemur catta): implications for the masculinization of
daughters.},
Journal = {Hormones and behavior},
Volume = {59},
Number = {4},
Pages = {417-427},
Year = {2011},
Month = {April},
url = {http://www.ncbi.nlm.nih.gov/pubmed/20932838},
Abstract = {Female ring-tailed lemurs (Lemur catta) are Malagasy
primates that are size monomorphic with males, socially
dominate males, and exhibit a long, pendulous clitoris,
channeled by the urethra. These masculine traits evoke
certain attributes of female spotted hyenas (Crocuta
crocuta) and draw attention to the potential role of
androgens in lemur sexual differentiation. Here, hormonal
correlates of prenatal development were assessed to explore
the possibility that maternal androgens may shape the
masculine morphological and behavioral features of
developing female lemurs. Maternal serum
17α-hydroxyprogesterone, dehydroepiandrosterone sulphate
(DHEA-S), ∆⁴ androstenedione (androst-4-ene-3,17,dione),
testosterone, and 17β-estradiol were charted throughout the
19 pregnancies of 11 ring-tailed lemurs. As in spotted
hyenas, lemur pregnancies were associated with an immediate
increase in androgen concentrations (implicating early
maternal derivation), followed by continued increases across
stages of gestation. Pregnancies that produced singleton
males, twin males, or mixed-sex twins were marked by greater
androgen and estrogen concentrations than were pregnancies
that produced singleton or twin females, especially in the
third trimester, implicating the fetal testes in late-term
steroid profiles. Concentrations of DHEA-S were mostly below
detectable limits, suggesting a minor role for the adrenals
in androgen biosynthesis. Androgen concentrations of
pregnant lemurs bearing female fetuses, although less than
those of pregnant hyenas, exceeded preconception and
postpartum values and peaked in the third trimester.
Although a maternal (and, on occasion, fraternal) source of
androgen may exist for fetal lemurs, further research is
required to confirm that these steroids would reach the
developing female and contribute to her masculinization.},
Doi = {10.1016/j.yhbeh.2010.09.011},
Key = {fds240197}
}
@article{fds240178,
Author = {Wallen, TW and Goodwin, TE and Moresco, A and Drea,
CM},
Title = {Prospecting for urinary chemical signals in binturongs
(Arctictis binturong)},
Journal = {ABSTRACTS OF PAPERS OF THE AMERICAN CHEMICAL
SOCIETY},
Volume = {241},
Pages = {1 pages},
Publisher = {AMER CHEMICAL SOC},
Year = {2011},
Month = {March},
ISSN = {0065-7727},
url = {http://gateway.webofknowledge.com/gateway/Gateway.cgi?GWVersion=2&SrcApp=PARTNER_APP&SrcAuth=LinksAMR&KeyUT=WOS:000291982800928&DestLinkType=FullRecord&DestApp=ALL_WOS&UsrCustomerID=47d3190e77e5a3a53558812f597b0b92},
Key = {fds240178}
}
@article{fds240198,
Author = {Place, NJ and Coscia, EM and Dahl, NJ and Drea, CM and Holekamp, KE and Roser, JF and Sisk, CL and Weldele, ML and Glickman,
SE},
Title = {The anti-androgen combination, flutamide plus finasteride,
paradoxically suppressed LH and androgen concentrations in
pregnant spotted hyenas, but not in males.},
Journal = {General and comparative endocrinology},
Volume = {170},
Number = {3},
Pages = {455-459},
Year = {2011},
Month = {February},
url = {http://www.ncbi.nlm.nih.gov/pubmed/21036174},
Abstract = {The androgen receptor blocker flutamide and the
5α-reductase inhibitor finasteride have been used in a
variety of species to investigate the ontogeny of sexual
dimorphisms by treating pregnant females or neonates at
critical periods of sexual differentiation. Likewise, we
have used these drugs to study the profound masculinization
of the external genitalia in female spotted hyenas. However,
a potential pitfall of administering flutamide, either alone
or in combination with finasteride, is that it maintains or
even raises plasma concentrations of luteinizing hormone
(LH) and testosterone (T), because negative feedback of the
hypothalamic-pituitary-gonadal axis is disrupted. Contrary
to expectations, when pregnant spotted hyenas were treated
with flutamide and finasteride (F&F), the concentrations of
T during late gestation were suppressed relative to values
in untreated dams. Herein, we further investigate the
paradoxical effects of F&F treatment on a battery of sex
hormones in spotted hyenas. Beyond the effects on T, we
found plasma concentrations of LH, estradiol, progesterone
and androstenedione (A4) were also significantly lower in
F&F-treated pregnant hyenas than in controls. Flutamide and
finasteride did not have similar effects on LH, T, and A4
concentrations in male hyenas. The paradoxical effect of F&F
treatment on LH and T concentrations in the maternal
circulation suggests that negative feedback control of
gonadotropin and androgen secretion may be modified in
spotted hyenas during pregnancy.},
Doi = {10.1016/j.ygcen.2010.10.016},
Key = {fds240198}
}
@article{fds240225,
Author = {Delbarco-Trillo, J and Burkert, BA and Goodwin, TE and Drea,
CM},
Title = {Night and day: the comparative study of strepsirrhine
primates reveals socioecological and phylogenetic patterns
in olfactory signals.},
Journal = {Journal of evolutionary biology},
Volume = {24},
Number = {1},
Pages = {82-98},
Year = {2011},
Month = {January},
url = {http://www.ncbi.nlm.nih.gov/pubmed/21091564},
Abstract = {Studies of chemical signals in vertebrates typically target
single species; however, a broader understanding of
olfactory communication may derive from comparative studies.
We collected urine from 12 species representing most
families of strepsirrhine primates--an excellent model clade
because of variation in scent marking and socioecology.
Using SPDE/GC-MS, we identified the volatile chemical
composition of male and female urine from six 'urine
marking' species and six glandular or 'non-urine marking'
species. We found no sex differences, but as predicted,
urine markers expressed the most chemically complex and
distinctive urine. More distantly related species had more
dissimilar urinary profiles, suggesting gradual signal
evolution. Reconstructing ancestral chemical profiles
revealed different evolutionary trajectories for urine and
non-urine markers. We suggest that urine marking is an
ancestral behaviour related to solitary, nocturnal living
and that parallel evolutionary shifts towards greater
reliance on derived glandular marking occurred in a family
(Lemuridae) characterized by diurnality and
sociality.},
Doi = {10.1111/j.1420-9101.2010.02145.x},
Key = {fds240225}
}
@article{fds240199,
Author = {Crawford, J and Boulet, M and Drea, CM},
Title = {Smelling wrong: Hormonal contraception in lemurs alters
critical female odour cues.},
Journal = {Proc Roy Soc, B},
Volume = {278},
Number = {1702},
Pages = {122-130},
Year = {2011},
url = {http://www.ncbi.nlm.nih.gov/pubmed/20667870},
Abstract = {Animals, including humans, use olfaction to assess potential
social and sexual partners. Although hormones modulate
olfactory cues, we know little about whether contraception
affects semiochemical signals and, ultimately, mate choice.
We examined the effects of a common contraceptive,
medroxyprogesterone acetate (MPA), on the olfactory cues of
female ring-tailed lemurs (Lemur catta) and the behavioural
response these cues generated in male conspecifics. The
genital odorants of contracepted females were dramatically
altered, falling well outside the range of normal female
variation: MPA decreased the richness and modified the
relative abundances of volatile chemicals expressed in
labial secretions. Comparisons between treatment groups
revealed several indicator compounds that could reliably
signal female reproductive status to conspecifics. MPA also
changed a female’s individual chemical ‘signature,’
while minimizing her chemical distinctiveness relative to
other contracepted females. Most remarkably, MPA degraded
the chemical patterns that encode honest information about
genetic constitution, including individual diversity
(heterozygosity) and pairwise relatedness to conspecifics.
Lastly, males preferentially investigated the odorants of
intact over contracepted females, clearly distinguishing
those with immediate reproductive potential. By altering the
olfactory cues that signal fertility, individuality, genetic
quality and relatedness, contraceptives may disrupt
intraspecific interactions in primates, including those
relevant to kin recognition and mate choice.},
Doi = {10.1098/rspb.2010.1203},
Key = {fds240199}
}
@article{fds240226,
Author = {Boulet, M and Crawford, JC and Charpentier, MJE and Drea,
CM},
Title = {Honest olfactory ornamentation in a female-dominant
primate.},
Journal = {Journal of evolutionary biology},
Volume = {23},
Number = {7},
Pages = {1558-1563},
Year = {2010},
Month = {July},
url = {http://www.ncbi.nlm.nih.gov/pubmed/20492092},
Abstract = {Sexual selection theory predicts that potential mates or
competitors signal their quality to conspecifics. Whereas
evidence of honest visual or vocal signals in males abounds,
evidence of honest signalling via scent or by females is
scarce. We previously showed that scent marks in male lemurs
seasonally encode information about individual
heterozygosity - a reliable predictor of immunocompetence
and survivorship. As female lemurs dominate males, compete
over resources, and produce sexually differentiated scent
marks that likely evolved via direct selection, here we
tested whether females also advertise genetic quality via
olfactory cues. During the breeding season specifically,
individual heterozygosity correlated negatively with the
diversity of fatty acids (FAs) expressed in labial
secretions and positively with the diversity of heavy FA
esters. As odour-gene relationships predictive of health and
survivorship emerged during a period critical to mate choice
and female competition, we posit that genital scent marks
function as honest olfactory ornaments in
females.},
Doi = {10.1111/j.1420-9101.2010.02007.x},
Key = {fds240226}
}
@article{fds240165,
Author = {Burkert, BA and Broederdorf, LJ and Hirwa, IH and Waldrip, ZJ and Goodwin, TE and Drea, CM},
Title = {Mammalian chemical communication: Comparative investigation
of urinary signals in prosimian primates},
Journal = {ABSTRACTS OF PAPERS OF THE AMERICAN CHEMICAL
SOCIETY},
Volume = {239},
Pages = {1 pages},
Publisher = {AMER CHEMICAL SOC},
Year = {2010},
Month = {March},
ISSN = {0065-7727},
url = {http://gateway.webofknowledge.com/gateway/Gateway.cgi?GWVersion=2&SrcApp=PARTNER_APP&SrcAuth=LinksAMR&KeyUT=WOS:000208189301154&DestLinkType=FullRecord&DestApp=ALL_WOS&UsrCustomerID=47d3190e77e5a3a53558812f597b0b92},
Key = {fds240165}
}
@article{fds240228,
Author = {Starling, AP and Charpentier, MJE and Fitzpatrick, C and Scordato,
ES and Drea, CM},
Title = {Seasonality, sociality, and reproduction: Long-term
stressors of ring-tailed lemurs (Lemur catta).},
Journal = {Hormones and behavior},
Volume = {57},
Number = {1},
Pages = {76-85},
Year = {2010},
Month = {January},
url = {http://www.ncbi.nlm.nih.gov/pubmed/19804779},
Abstract = {Fecal glucocorticoid (fGC) concentrations are reliable,
non-invasive indices of physiological stress that provide
insight into an animal's energetic and social demands. To
better characterize the long-term stressors in adult members
of a female-dominant, seasonally breeding species - the
ring-tailed lemur (Lemur catta) - we first validated fecal
samples against serum samples and then examined the
relationship between fGC concentrations and seasonal,
social, demographic, genetic, and reproductive variables.
Between 1999 and 2006, we collected 1386 fecal samples from
32 adult, semi-free-ranging animals of both sexes. In males
and non-pregnant, non-lactating females, fGC concentrations
were significantly elevated during the breeding season,
specifically during periods surrounding known conceptions.
Moreover, group composition (e.g., multi-male versus
one-male) significantly predicted the fGC concentrations of
males and females in all reproductive states. In particular,
the social instability introduced by intra-male competition
likely created a stressor for all animals. We found no
relationship, however, between fGC and the sex, age, or
heterozygosity of animals. In reproducing females, fGC
concentrations were significantly greater during lactation
than during the pre-breeding period. During pregnancy, fGC
concentrations were elevated in mid-ranking dams, relative
to dominant or subordinate dams, and significantly greater
during the third trimester than during the first or second
trimesters. Thus, in the absence of nutritional stressors,
social dominance was a relatively poor predictor of fGC in
this female-dominant species. Instead, the animals were
maximally challenged by their social circumstances and
reproductive events-males by competition for mating
opportunities and females by late-term gestation and
lactation.},
Doi = {10.1016/j.yhbeh.2009.09.016},
Key = {fds240228}
}
@article{fds240227,
Author = {Charpentier, MJE and Crawford, J and Boulet, M and Drea,
CM},
Title = {Message 'scent': lemurs detect the genetic relatedness and
quality of conspecifics via olfactory cues},
Journal = {Animal Behaviour},
Volume = {80},
Number = {1},
Pages = {101-108},
Publisher = {Elsevier BV},
Year = {2010},
ISSN = {0003-3472},
url = {http://dx.doi.org/10.1016/j.anbehav.2010.04.005},
Abstract = {To enhance the fitness benefits of social and sexual
interaction, animals should be able to decipher information
about the genetic makeup of conspecifics. The use of
relative criteria to estimate genetic relatedness could
facilitate nepotism or inbreeding avoidance, and the use of
absolute criteria to estimate genetic quality could help
identify the fittest competitor or the best mate. For
animals to process trade-offs between relatedness and
quality, however, both relative and absolute genetic
information must be concurrently available and detectable by
conspecifics. Although there is increasing evidence to
suggest that animals make genetically informed decisions
about their partners, and may even process trade-offs, we
understand relatively little about the sensory mechanisms
informing these decisions. In previous analyses of the
olfactory signals of ring-tailed lemurs (Lemur catta), we
showed that both scrotal and labial secretions seasonally
encode chemical information about (1) pairwise genetic
relatedness, within and between the sexes, and (2)
individual heterozygosity. Here, using a signaller-receiver
paradigm, we conducted behavioural bioassays to test if male
and female lemurs are sensitive to these olfactory sources
of genetic information in unfamiliar conspecifics. As the
lemurs discriminated conspecific glandular secretions by
pairwise relatedness and individual heterozygosity, volatile
olfactory signals can be used by both sexes to concurrently
process relative and absolute genetic information about
conspecifics. Beyond supporting an olfactory mechanism of
kin discrimination and mate choice in a primate, we suggest
that animals could use olfactory processing to trade off
between selection for the most compatible partner versus the
most genetically diverse partner.},
Doi = {10.1016/j.anbehav.2010.04.005},
Key = {fds240227}
}
@article{fds240190,
Author = {Boulet, M and Charpentier, MJE and Drea, CM},
Title = {Decoding an olfactory mechanism of kin recognition and
inbreeding avoidance in a primate.},
Journal = {BMC evolutionary biology},
Volume = {9},
Pages = {281},
Year = {2009},
Month = {December},
url = {http://www.ncbi.nlm.nih.gov/pubmed/19958525},
Abstract = {<h4>Background</h4>Like other vertebrates, primates
recognize their relatives, primarily to minimize inbreeding,
but also to facilitate nepotism. Although associative,
social learning is typically credited for discrimination of
familiar kin, discrimination of unfamiliar kin remains
unexplained. As sex-biased dispersal in long-lived species
cannot consistently prevent encounters between unfamiliar
kin, inbreeding remains a threat and mechanisms to avoid it
beg explanation. Using a molecular approach that combined
analyses of biochemical and microsatellite markers in 17
female and 19 male ring-tailed lemurs (Lemur catta), we
describe odor-gene covariance to establish the feasibility
of olfactory-mediated kin recognition.<h4>Results</h4>Despite
derivation from different genital glands, labial and scrotal
secretions shared about 170 of their respective 338 and 203
semiochemicals. In addition, these semiochemicals encoded
information about genetic relatedness within and between the
sexes. Although the sexes showed opposite seasonal patterns
in signal complexity, the odor profiles of related
individuals (whether same-sex or mixed-sex dyads) converged
most strongly in the competitive breeding season. Thus, a
strong, mutual olfactory signal of genetic relatedness
appeared specifically when such information would be crucial
for preventing inbreeding. That weaker signals of genetic
relatedness might exist year round could provide a mechanism
to explain nepotism between unfamiliar kin.<h4>Conclusion</h4>We
suggest that signal convergence between the sexes may
reflect strong selective pressures on kin recognition,
whereas signal convergence within the sexes may arise as its
by-product or function independently to prevent competition
between unfamiliar relatives. The link between an
individual's genome and its olfactory signals could be
mediated by biosynthetic pathways producing polymorphic
semiochemicals or by carrier proteins modifying the
individual bouquet of olfactory cues. In conclusion, we
unveil a possible olfactory mechanism of kin recognition
that has specific relevance to understanding inbreeding
avoidance and nepotistic behavior observed in free-ranging
primates, and broader relevance to understanding the
mechanisms of vertebrate olfactory communication.},
Doi = {10.1186/1471-2148-9-281},
Key = {fds240190}
}
@article{fds240200,
Author = {Drea, CM and Carter, AN},
Title = {Cooperative problem solving in a social carnivore},
Journal = {Animal Behaviour},
Volume = {78},
Number = {4},
Pages = {967-977},
Publisher = {Elsevier BV},
Year = {2009},
Month = {October},
ISSN = {0003-3472},
url = {http://dx.doi.org/10.1016/j.anbehav.2009.06.030},
Abstract = {Numerous field researchers have described cooperative
hunting in social carnivores, but experimental evidence of
cooperative problem solving typically derives from
laboratory studies of nonhuman primates. We present the
first experimental evidence of cooperation in a social
carnivore, the spotted hyaena, Crocuta crocuta. Eight
captive hyaenas, paired in 13 combinations, coordinated
their behaviour temporally and spatially to solve
cooperation tasks that modelled group-hunting strategies.
Unlike many primates that cooperate infrequently or require
extensive shaping, spotted hyaenas displayed a natural
aptitude for teamwork: all teams achieved success rapidly,
repeatedly, and without specific training. Social influences
on cooperative performance included an audience effect that
could influence party formation and hunting success in the
wild. Performance also varied across dyads, notably with
rank-related aggression between partners impairing
performance. Efficiency improved as partners increasingly
attended to one another and coordinated their actions.
Lastly, experienced cooperators modified their behaviour to
accommodate a naïve companion, using visual monitoring and
tracking to promote coordination. We suggest that social
carnivores should be considered relevant models for the
study of cooperative problem solving, as their abilities
provide a comparative framework for testing theories about
the mechanisms of social learning and the evolution of
intelligence. © 2009 The Association for the Study of
Animal Behaviour.},
Doi = {10.1016/j.anbehav.2009.06.030},
Key = {fds240200}
}
@article{fds240207,
Author = {Drea, CM},
Title = {Endocrine mediators of masculinization in female
mammals},
Journal = {Current Directions in Psychological Science},
Volume = {18},
Number = {4},
Pages = {221-226},
Publisher = {SAGE Publications},
Year = {2009},
Month = {August},
ISSN = {0963-7214},
url = {http://dx.doi.org/10.1111/j.1467-8721.2009.01640.x},
Abstract = {Most mammal species show traditional patterns of sexual
dimorphism (e.g., greater male size and aggression), the
proximal mechanism of which involves the male's greater pre-
and postnatal exposure to circulating androgens. But in
several species, females diverge from the traditional
pattern, converging on the male form or even reversing
sexual dimorphisms. Such "masculinized" females might show
elongation of the clitoris, enhanced body size, and
aggressively mediated social dominance over males, and they
are interesting case studies for examining the role of
androgens in females. This review addresses our
understanding of the mediating mechanisms of morphological
and behavioral development in both traditional and
exceptional mammal species. Although certain lines of
evidence implicate testosterone in female masculinization,
the role for sex steroids in female development remains
unclear. The results call for continued study of both
hormonal and nonhormonal mechanisms of sexual
differentiation, particularly focused on active processes of
feminine development. © 2009 Association for Psychological
Science.},
Doi = {10.1111/j.1467-8721.2009.01640.x},
Key = {fds240207}
}
@article{fds240180,
Author = {Crawford, JC and Charpentier, MJE and Boulet, M and Drea,
CM},
Title = {Lemurs Discriminate the Scent of Conspecifics Based on
Individual Heterozygosity and Pairwise Relatedness},
Journal = {INTEGRATIVE AND COMPARATIVE BIOLOGY},
Volume = {49},
Pages = {E41-E41},
Publisher = {OXFORD UNIV PRESS INC},
Year = {2009},
Month = {February},
ISSN = {1540-7063},
url = {http://gateway.webofknowledge.com/gateway/Gateway.cgi?GWVersion=2&SrcApp=PARTNER_APP&SrcAuth=LinksAMR&KeyUT=WOS:000268808800163&DestLinkType=FullRecord&DestApp=ALL_WOS&UsrCustomerID=47d3190e77e5a3a53558812f597b0b92},
Key = {fds240180}
}
@article{fds240189,
Author = {Leonhardt, SD and Tung, J and Camden, JB and Leal, M and Drea,
CM},
Title = {Seeing red: Behavioral evidence of trichromatic color vision
in strepsirrhine primates},
Journal = {Behavioral Ecology},
Volume = {20},
Number = {1},
Pages = {1-12},
Publisher = {Oxford University Press (OUP)},
Year = {2009},
Month = {January},
ISSN = {1045-2249},
url = {http://dx.doi.org/10.1093/beheco/arn106},
Abstract = {Among primates, catarrhines (Old World monkeys and apes) and
certain platyrrhines (New World monkeys) possess
trichromatic color vision, which might confer important
evolutionary advantages, particularly during foraging.
Recently, a polymorphism has been shown to shift the
spectral sensitivity of the X-linked opsin protein in
certain strepsirrhines (e.g., Malagasy lemurs); however, its
behavioral significance remains unknown. We assign genotypes
at the X-linked variant to 45 lemurs, representing 4
species, and test if the genetic capacity for trichromacy
impacts foraging performance, particularly under green
camouflage conditions in which red detection can be
advantageous. We confirm polymorphism at the critical site
in sifakas and ruffed lemurs and fail to find this
polymorphism in collared lemurs and ring-tailed lemurs. We
show that this polymorphism may be linked to "behavioral
trichromacy" in heterozygous ruffed lemurs but find no
comparable evidence in a single heterozygous sifaka. Despite
their putative dichromatic vision, female collared lemurs
were surprisingly efficient at retrieving both red and green
food items under camouflage conditions. Thus,
species-specific feeding ecologies may be as important as
trichromacy in influencing foraging behavior. Although the
lemur opsin polymorphism produced measurable behavioral
effects in at least one species, the ruffed lemur, these
effects were modest, consistent with the modest shift in
spectral sensitivity. Additionally, the magnitude of these
effects varied across individuals of the same genotype,
emphasizing the need for combined genetic and behavioral
studies of trichromatic vision. We conclude that trichromacy
may be only one of several routes toward increased foraging
efficiency in visually complex environments. © The Author
2008. Published by Oxford University Press on behalf of the
International Society for Behavioral Ecology. All rights
reserved.},
Doi = {10.1093/beheco/arn106},
Key = {fds240189}
}
@article{fds240206,
Author = {Charpentier, MJE and Boulet, M and Drea, CM},
Title = {Smelling right: the scent of male lemurs advertises genetic
quality and relatedness.},
Journal = {Molecular ecology},
Volume = {17},
Number = {14},
Pages = {3225-3233},
Year = {2008},
Month = {July},
url = {http://www.ncbi.nlm.nih.gov/pubmed/18565115},
Abstract = {Sexual selection theory predicts that competitors or
potential mates signal their quality or relatedness to
conspecifics. Researchers have focused on visual or auditory
modes of signal transmission; however, the importance of
olfactory indicators is gaining recognition. Using a primate
model and a new integrative analytical approach, we provide
the first evidence relating male olfactory cues to
individual genome-wide heterozygosity and to the genetic
distance between individuals. The relationships between male
semiochemical profiles and genetic characteristics are
apparent only during the highly competitive and stressful
breeding season. As heterozygosity accurately predicts
health and survivorship in this population, we identify
scrotal olfactory cues as honest indicators of male quality,
with relevance possibly to both sexes. Beyond showing that
semiochemicals could underlie kin recognition and nepotism,
we provide a putative olfactory mechanism to guide male-male
competition and female mate choice.},
Doi = {10.1111/j.1365-294x.2008.03831.x},
Key = {fds240206}
}
@article{fds240204,
Author = {Drea, CM and Weil, A},
Title = {External genital morphology of the ring-tailed lemur (Lemur
catta): females are naturally "masculinized".},
Journal = {Journal of morphology},
Volume = {269},
Number = {4},
Pages = {451-463},
Year = {2008},
Month = {April},
ISSN = {0362-2525},
url = {http://www.ncbi.nlm.nih.gov/pubmed/17972270},
Abstract = {The extravagance and diversity of external genitalia have
been well characterized in male primates; however, much less
is known about sex differences or variation in female form.
Our study represents a departure from traditional
investigations of primate reproductive anatomy because we 1)
focus on external rather than internal genitalia, 2) measure
both male and female structures, and 3) examine a
strepsirrhine rather than an anthropoid primate. The
subjects for morphological study were 21 reproductively
intact, adult ring-tailed lemurs (Lemur catta), including 10
females and 11 males, two of which (one per sex)
subsequently died of natural causes and also served as
specimens for gross anatomical dissection. Male external
genitalia presented a typical masculine configuration, with
a complex distal penile morphology. In contrast, females
were unusual among mammals, presenting an enlarged,
pendulous external clitoris, tunneled by the urethra.
Females had a shorter anogenital distance and a larger
urethral meatus than did males, but organ diameter and
circumference showed no sex differences. Dissection
confirmed these characterizations. Noteworthy in the male
were the presence of a "levator penis" muscle and
discontinuity in the corpus spongiosum along the penile
shaft; noteworthy in the female were an elongated clitoral
shaft and glans clitoridis. The female urethra, while
incorporated within the clitoral body, was not surrounded by
erectile tissue, as we detected no corpus spongiosum. The os
clitoridis was 43% the length and 24% the height of the os
penis. On the basis of these first detailed descriptions of
strepsirrhine external genitalia (for either sex), we
characterize those of the female ring-tailed lemur as
moderately "masculinized." Our results highlight certain
morphological similarities and differences between
ring-tailed lemurs and the most male-like of female mammals,
the spotted hyena (Crocuta crocuta), and call attention to a
potential hormonal mechanism of "masculinization" in female
lemur development.},
Doi = {10.1002/jmor.10594},
Key = {fds240204}
}
@article{fds240201,
Author = {Charpentier, MJE and Williams, CV and Drea, CM},
Title = {Inbreeding depression in ring-tailed lemurs (Lemur catta):
Genetic diversity predicts parasitism, immunocompetence, and
survivorship},
Journal = {Conservation Genetics},
Volume = {9},
Number = {6},
Pages = {1605-1615},
Publisher = {Springer Nature},
Year = {2008},
Month = {January},
ISSN = {1566-0621},
url = {http://dx.doi.org/10.1007/s10592-007-9499-4},
Abstract = {The consequences of inbreeding have been well studied in a
variety of taxa, revealing that inbreeding has major
negative impacts in numerous species, both in captivity and
in the wild; however, as trans-generational health data are
difficult to obtain for long-lived, free-ranging species,
similar analyses are generally lacking for nonhuman
primates. Here, we examined the long-term effects of
inbreeding on numerous health estimates in a captive colony
of ring-tailed lemurs (Lemur catta), housed under
semi-natural conditions. This vulnerable strepsirrhine
primate is endemic to Madagascar, a threatened hotspot of
biodiversity; consequently, this captive population
represents an important surrogate. Despite significant
attention to maintaining the genetic diversity of captive
animals, breeding colonies invariably suffer from various
degrees of inbreeding. We used neutral heterozygosity as an
estimate of inbreeding and showed that our results reflect
genome-wide inbreeding, rather than local genetic effects.
In particular, we found that genetic diversity affects
several fitness correlates, including the prevalence and
burden of Cuterebra parasites and a third (N = 6) of the
blood parameters analyzed, some of which reflect
immunocompetence. As a final validation of inbreeding
depression in this captive colony, we showed that, compared
to outbred individuals, inbred lemurs were more likely to
die earlier from diseases. Through these analyses, we
highlight the importance of monitoring genetic variation in
captive animals-a key objective for conservation
geneticists-and provide insight into the potential negative
consequences faced by small or isolated populations in the
wild. © 2008 Springer Science+Business Media
B.V.},
Doi = {10.1007/s10592-007-9499-4},
Key = {fds240201}
}
@article{fds240174,
Author = {Drea, CM and Scordato, ES},
Title = {Olfactory Communication in the Ringtailed Lemur (Lemur
catta): Form and Function of Multimodal Signals},
Volume = {11},
Pages = {91-102},
Booktitle = {Chemical Signals in Vertebrates},
Publisher = {Springer New York},
Editor = {J. Hurst and R.J. Beynon and S.C. Roberts and T.
Wyatt},
Year = {2008},
ISBN = {9780387739441},
url = {http://gateway.webofknowledge.com/gateway/Gateway.cgi?GWVersion=2&SrcApp=PARTNER_APP&SrcAuth=LinksAMR&KeyUT=WOS:000251798000009&DestLinkType=FullRecord&DestApp=ALL_WOS&UsrCustomerID=47d3190e77e5a3a53558812f597b0b92},
Abstract = {To better understand the relation between form and function
in the complex olfactory com-munication system of the
ringtailed lemur (Lemur catta), we integrated observational,
experimental, and chemical approaches applied to a
population of semi free-ranging animals at the Duke Lemur
Center in Durham, North Carolina. Our aim was to examine
sex-role reversal in the expression and function of scent
marking and unravel the contribution of multimodal
components of information transfer, with the unifying
framework for all three avenues of our research being that
multiplicity of form implies multiplicity of
function.},
Doi = {10.1007/978-0-387-73945-8_8},
Key = {fds240174}
}
@article{fds240168,
Author = {Drea, CM},
Title = {Hormonal and experiential regulation of social dominance in
macaques, hyenas, and lemurs},
Journal = {AMERICAN JOURNAL OF PRIMATOLOGY},
Volume = {69},
Pages = {125-125},
Publisher = {WILEY-LISS},
Year = {2007},
Month = {June},
ISSN = {0275-2565},
url = {http://gateway.webofknowledge.com/gateway/Gateway.cgi?GWVersion=2&SrcApp=PARTNER_APP&SrcAuth=LinksAMR&KeyUT=WOS:000247093700193&DestLinkType=FullRecord&DestApp=ALL_WOS&UsrCustomerID=47d3190e77e5a3a53558812f597b0b92},
Key = {fds240168}
}
@article{fds240169,
Author = {Drea, CM},
Title = {How to study socially biased learning in primates? Trends
and future directions},
Journal = {AMERICAN JOURNAL OF PRIMATOLOGY},
Volume = {69},
Pages = {78-79},
Publisher = {WILEY-LISS},
Year = {2007},
Month = {June},
ISSN = {0275-2565},
url = {http://gateway.webofknowledge.com/gateway/Gateway.cgi?GWVersion=2&SrcApp=PARTNER_APP&SrcAuth=LinksAMR&KeyUT=WOS:000247093700100&DestLinkType=FullRecord&DestApp=ALL_WOS&UsrCustomerID=47d3190e77e5a3a53558812f597b0b92},
Key = {fds240169}
}
@article{fds240170,
Author = {Kwatra, SG and Drea, CM},
Title = {Proteomic analysis of ringtailed lemur scent gland
secretions: Glandular- and individual-specific protein
profiles},
Journal = {AMERICAN JOURNAL OF PRIMATOLOGY},
Volume = {69},
Pages = {108-109},
Publisher = {WILEY-LISS},
Year = {2007},
Month = {June},
ISSN = {0275-2565},
url = {http://gateway.webofknowledge.com/gateway/Gateway.cgi?GWVersion=2&SrcApp=PARTNER_APP&SrcAuth=LinksAMR&KeyUT=WOS:000247093700160&DestLinkType=FullRecord&DestApp=ALL_WOS&UsrCustomerID=47d3190e77e5a3a53558812f597b0b92},
Key = {fds240170}
}
@article{fds240203,
Author = {Scordato, ES and Dubay, G and Drea, CM},
Title = {Chemical composition of scent marks in the ringtailed lemur
(Lemur catta): glandular differences, seasonal variation,
and individual signatures.},
Journal = {Chemical senses},
Volume = {32},
Number = {5},
Pages = {493-504},
Year = {2007},
Month = {June},
ISSN = {0379-864X},
url = {http://www.ncbi.nlm.nih.gov/pubmed/17488747},
Abstract = {The apocrine and sebaceous scent glands of ringtailed lemurs
(Lemur catta) appear to serve different social functions. In
behavioral experiments, lemurs modulate their responses to
scent marks based on the type of odorant, their own
physiological state, the signaler's physiological state, and
prior social experience. To examine variation in odorant
chemistry relative to olfactory behavior, we used gas
chromatography and mass spectrometry to analyze over 86
samples of glandular secretion collected over 2 years from
15 adult lemurs. Labial and scrotal secretions contained
organic acids and esters, whereas male brachial secretions
were composed almost entirely of squalene and cholesterol
derivatives. Principal component and linear discriminant
analyses revealed glandular, individual-specific, and
seasonal variation in chemical profiles but no relationship
to the signaler's social status. The chemical composition of
the various secretions provides further clues about the
function of the different glands: the higher molecular
weight compounds in genital and brachial secretions may
increase signal longevity and provide lasting information to
conspecifics, consistent with a role in advertising resource
ownership or reproductive state. Conversely, the lower
molecular weight compounds of antebrachial secretions
produce ephemeral signals used primarily in social dominance
displays and require integration of multiple sensory
modalities for effective signal transmission.},
Doi = {10.1093/chemse/bjm018},
Key = {fds240203}
}
@article{fds240205,
Author = {Drea, CM},
Title = {Sex and seasonal differences in aggression and steroid
secretion in Lemur catta: are socially dominant females
hormonally 'masculinized'?},
Journal = {Hormones and behavior},
Volume = {51},
Number = {4},
Pages = {555-567},
Year = {2007},
Month = {April},
ISSN = {0018-506X},
url = {http://www.ncbi.nlm.nih.gov/pubmed/17382329},
Abstract = {Female social dominance characterizes many strepsirrhine
primates endemic to Madagascar, but currently there is no
comprehensive explanation for how or why female lemurs
routinely dominate males. Reconstructing the evolutionary
pressures that may have shaped female dominance depends on
better understanding the mechanism of inheritance, variation
in trait expression, and correlating variables. Indeed,
relative to males, many female lemurs also display delayed
puberty, size monomorphism, and 'masculinized' external
genitalia. As in the spotted hyena (Crocuta crocuta), a
species characterized by extreme masculinization of the
female, this array of traits focuses attention on the role
of androgens in female development. Consequently, I examined
endocrine profiles and social interaction in the ringtailed
lemur (Lemur catta) to search for a potential source of
circulating androgen in adult females and an endocrine
correlate of female dominance or its proxy, aggression. I
measured serum androstenedione (A(4)), testosterone (T), and
estradiol (E(2)) in reproductively intact, adult lemurs (10
females; 12 males) over four annual cycles. Whereas T
concentrations in males far exceeded those in females, A(4)
concentrations were only slightly greater in males than in
females. In both sexes, A(4) and T were positively
correlated, implicating the Delta(4)-biosynthetic pathway.
Moreover, seasonal changes in reproductive function in both
sexes coincided with seasonal changes in behavior, with A(4)
and T in males versus A(4) and E(2) in females increasing
during periods marked by heightened aggression. Therefore,
A(4) and/or E(2) may be potentially important steroidal
sources in female lemurs that could modulate aggression and
underlie a suite of masculinized features.},
Doi = {10.1016/j.yhbeh.2007.02.006},
Key = {fds240205}
}
@article{fds240202,
Author = {Scordato, ES and Drea, CM},
Title = {Scents and sensibility: information content of olfactory
signals in the ringtailed lemur, Lemur catta},
Journal = {Animal Behaviour},
Volume = {73},
Number = {2},
Pages = {301-314},
Publisher = {Elsevier BV},
Year = {2007},
Month = {February},
ISSN = {0003-3472},
url = {http://dx.doi.org/10.1016/j.anbehav.2006.08.006},
Abstract = {The function of olfactory signalling in social species is
less well understood than in asocial species. Consequently,
we examined olfactory communication in the ringtailed lemur,
a socially complex primate that retains a functional
vomeronasal organ, has well-developed scent glands and shows
a suite of scent-marking behaviour. To assess the
information content of different types of scent gland
secretions, we decoupled olfactory cues from the visual and
behavioural modalities with which scent marking is normally
associated. We presented male and female subjects (signal
receivers) with a series of choice tests between odours
derived from conspecific donors (signal senders) varying by
sex, age, social status and reproductive condition. We
additionally examined the influence of the receivers'
reproductive state and familiarity with the signaller. The
reproductive condition, social status and familiarity of
senders and receivers affected signal transmission;
specifically, male receivers attended most to the odours of
conspecifics in breeding condition and to the odours of
familiar, dominant animals. By contrast, females varied
their responses according to both their own reproductive
state and that of the sender. Based on male and female
patterns of countermarking, we suggest that scent marking
serves a function in intergroup spacing and intrasexual
competition for both sexes, as might be expected in a
female-dominant species. By contrast, minimal female
interest in male odours counters a female mate choice
function for scent marking in this species. Nevertheless,
scent marks are critical to male-male competition and,
therefore, may be subject to sexual selection. © 2006 The
Association for the Study of Animal Behaviour.},
Doi = {10.1016/j.anbehav.2006.08.006},
Key = {fds240202}
}
@article{fds240208,
Author = {Glickman, SE and Cunha, GR and Drea, CM and Conley, AJ and Place,
NJ},
Title = {Mammalian sexual differentiation: lessons from the spotted
hyena.},
Journal = {Trends in endocrinology and metabolism: TEM},
Volume = {17},
Number = {9},
Pages = {349-356},
Year = {2006},
Month = {November},
ISSN = {1043-2760},
url = {http://www.ncbi.nlm.nih.gov/pubmed/17010637},
Abstract = {Female spotted hyenas (Crocuta crocuta) are the only female
mammals that lack an external vaginal opening. Mating and
birth take place through a urogenital canal that exits at
the tip of a hypertrophied clitoris. This 'masculine'
phenotype spurred a search for an alternate source of fetal
androgens. Although androstenedione from the maternal ovary
is readily metabolized to testosterone by the hyena
placenta, formation of the penile clitoris and scrotum
appear to be largely androgen independent. However,
secretions from the fetal testes underlie sex differences in
the genitalia and central nervous system that are essential
for male reproduction. Naturally circulating androgens,
acting prenatally, reduce reproductive success in adult
female spotted hyenas. Effects on aggression and dominance
might offset these reproductive 'costs' of female
androgenization in utero.},
Doi = {10.1016/j.tem.2006.09.005},
Key = {fds240208}
}
@article{fds240224,
Author = {Drea, CM},
Title = {Studying primate learning in group contexts: Tests of social
foraging, response to novelty, and cooperative problem
solving.},
Journal = {Methods (San Diego, Calif.)},
Volume = {38},
Number = {3},
Pages = {162-177},
Year = {2006},
Month = {March},
ISSN = {1046-2023},
url = {http://www.ncbi.nlm.nih.gov/pubmed/16458018},
Keywords = {Primate cognition; Social learning; Social foraging;
Discrimination learning; Response to novelty; Neophobia;
Cooperation; Problem-solving},
Abstract = {Learning commonly refers to the modification of behavior
through experience, whereby an animal gains information
about stimulus-response contingencies from interacting with
its physical environment. Social learning, on the other
hand, occurs when the same information originates, not from
the animal's personal experience, but from the actions of
others. Socially biased learning is the 'collective outcome
of interacting physical, social, and individual factors' [D.
Fragaszy, E. Visalberghi, Learn. Behav. 32 (2004) 24-35.]
(see p. 24). Mounting interest in animal social learning has
brought with it certain innovations in animal testing
procedures. Variants of the observer-demonstrator and
cooperation paradigms, for instance, have been used widely
in captive settings to examine the transmission or
coordination of behavior, respectively, between two animals.
Relatively few studies, however, have examined social
learning in more complex group settings and even fewer have
manipulated the social environment to empirically test the
effect of group dynamics on problem solving. The present
paper outlines procedures for group testing captive
non-human primates, in spacious arenas, to evaluate the
social modulation of learning and performance. These methods
are illustrated in the context of (1) naturalistic social
foraging problems, modeled after traditional visual
discrimination paradigms, (2) response to novel objects and
novel extractive foraging tasks, and (3) cooperative problem
solving. Each example showcases the benefits of
experimentally manipulating social context to compare an
animal's performance in intact groups (or even pairs)
against its performance under different social
circumstances. Broader application of group testing
procedures and manipulation of group composition promise to
provide meaningful insight into socially biased
learning.},
Doi = {10.1016/j.ymeth.2005.12.001},
Key = {fds240224}
}
@article{fds240177,
Author = {Drea, CM},
Title = {Morphological and hormonal correlates of 'masculinization'
in ringtailed lemurs (Lemur catta).},
Journal = {AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY},
Pages = {85-85},
Publisher = {WILEY-LISS},
Year = {2006},
Month = {January},
ISSN = {0002-9483},
url = {http://gateway.webofknowledge.com/gateway/Gateway.cgi?GWVersion=2&SrcApp=PARTNER_APP&SrcAuth=LinksAMR&KeyUT=WOS:000235661100123&DestLinkType=FullRecord&DestApp=ALL_WOS&UsrCustomerID=47d3190e77e5a3a53558812f597b0b92},
Key = {fds240177}
}
@article{fds240166,
Author = {Drea, CM},
Title = {Could female ringtailed lemurs be masculinized by maternal
androgens?},
Journal = {INTEGRATIVE AND COMPARATIVE BIOLOGY},
Volume = {45},
Number = {6},
Pages = {989-989},
Publisher = {OXFORD UNIV PRESS INC},
Year = {2005},
Month = {December},
ISSN = {1540-7063},
url = {http://gateway.webofknowledge.com/gateway/Gateway.cgi?GWVersion=2&SrcApp=PARTNER_APP&SrcAuth=LinksAMR&KeyUT=WOS:000235337600139&DestLinkType=FullRecord&DestApp=ALL_WOS&UsrCustomerID=47d3190e77e5a3a53558812f597b0b92},
Key = {fds240166}
}
@article{fds240172,
Author = {Roth, JD and Wiesel, I and Drea, CM},
Title = {Variation in seal consumption by brown hyenas in the Namib
desert estimated using stable isotopes},
Journal = {INTEGRATIVE AND COMPARATIVE BIOLOGY},
Volume = {45},
Number = {6},
Pages = {1065-1065},
Publisher = {OXFORD UNIV PRESS INC},
Year = {2005},
Month = {December},
ISSN = {1540-7063},
url = {http://gateway.webofknowledge.com/gateway/Gateway.cgi?GWVersion=2&SrcApp=PARTNER_APP&SrcAuth=LinksAMR&KeyUT=WOS:000235337600443&DestLinkType=FullRecord&DestApp=ALL_WOS&UsrCustomerID=47d3190e77e5a3a53558812f597b0b92},
Key = {fds240172}
}
@article{fds240175,
Author = {Scordato, ES and Drea, CM},
Title = {Sex-specific variation in ringtailed lemur Lemur catta
olfactory communication},
Journal = {INTEGRATIVE AND COMPARATIVE BIOLOGY},
Volume = {45},
Number = {6},
Pages = {1070-1070},
Publisher = {OXFORD UNIV PRESS INC},
Year = {2005},
Month = {December},
ISSN = {1540-7063},
url = {http://gateway.webofknowledge.com/gateway/Gateway.cgi?GWVersion=2&SrcApp=PARTNER_APP&SrcAuth=LinksAMR&KeyUT=WOS:000235337600463&DestLinkType=FullRecord&DestApp=ALL_WOS&UsrCustomerID=47d3190e77e5a3a53558812f597b0b92},
Key = {fds240175}
}
@article{fds240188,
Author = {Drea, CM},
Title = {Bateman revisited: the reproductive tactics of female
primates.},
Journal = {Integrative and comparative biology},
Volume = {45},
Series = {Integrative and Comparative Biology},
Number = {5},
Pages = {915-923},
Year = {2005},
Month = {November},
ISSN = {1540-7063},
url = {http://www.ncbi.nlm.nih.gov/pubmed/21676842},
Abstract = {The breeding system of an animal population is thought to
depend on the ability of one sex (usually the male) to
acquire mates, either directly through association with
females or indirectly through defense of the resources
desired by females. The sex that contributes most to infant
care (usually the female) is constrained by parental
involvement and thereby limits reproduction of the opposite
sex. Accordingly, males, but not females, enhance their
reproductive success by acquiring additional mates. This
classical view has emphasized the role of male-male
competition in sexual selection, at the expense of fully
exploring the potential for female choice. A more recent
shift in focus has revealed substantial variation in female
reproductive success and increasingly accentuates the
importance of female intrasexual competition and male mate
choice. A comparative review of primate reproduction,
therefore, challenges expectations of male control and
female compliance, and calls for a comprehensive treatment
of costs and benefits that extends beyond conventional
mention of heavy female investment versus male negligence or
absenteeism. For individuals that manipulate their social
environment or reproductive output, consideration of more
subtle, even cryptic, aspects of female behavior and
physiology (e.g., social strategizing, sexual solicitation
or rejection, sexual advertisement or concealed ovulation,
multiple mating, and reproductive failure) raises the
question of whether females can be effectively
'monopolized.' Widespread patterns that counter Bateman's
paradigm call for a reexamination of the predictions
generated by dichotomizing gametes into 'expensive eggs' and
'cheap sperm,' and encourage continued mechanistic research
focused on conception quality rather than
quantity.},
Doi = {10.1093/icb/45.5.915},
Key = {fds240188}
}
@article{fds240162,
Author = {Place, NJ and Coscia, EM and Dahl, NJ and Drea, CM and Holekamp, KE and Sisk, CL and Weldele, ML and Glickman, SE},
Title = {Paradoxical effects of maximal androgen blockade on sex
hormone concentrations in pregnant spotted hyenas, Crocuta
crocuta.},
Journal = {BIOLOGY OF REPRODUCTION},
Pages = {123-123},
Publisher = {SOC STUDY REPRODUCTION},
Year = {2005},
Month = {January},
ISSN = {0006-3363},
url = {http://gateway.webofknowledge.com/gateway/Gateway.cgi?GWVersion=2&SrcApp=PARTNER_APP&SrcAuth=LinksAMR&KeyUT=WOS:000230556300247&DestLinkType=FullRecord&DestApp=ALL_WOS&UsrCustomerID=47d3190e77e5a3a53558812f597b0b92},
Key = {fds240162}
}
@article{fds240167,
Author = {Drea, CM},
Title = {Bateman revisited: Sexually assertive female primates and
their cryptic reproductive tactics},
Journal = {INTEGRATIVE AND COMPARATIVE BIOLOGY},
Volume = {43},
Number = {6},
Pages = {915-915},
Publisher = {SOC INTEGRATIVE COMPARATIVE BIOLOGY},
Year = {2003},
Month = {December},
ISSN = {1540-7063},
url = {http://gateway.webofknowledge.com/gateway/Gateway.cgi?GWVersion=2&SrcApp=PARTNER_APP&SrcAuth=LinksAMR&KeyUT=WOS:000222235200450&DestLinkType=FullRecord&DestApp=ALL_WOS&UsrCustomerID=47d3190e77e5a3a53558812f597b0b92},
Key = {fds240167}
}
@book{fds240163,
Author = {Drea, CM and Frank, LG},
Title = {The social complexity of spotted hyenas},
Journal = {ANIMAL SOCIAL COMPLEXITY},
Pages = {121-+},
Booktitle = {Animal Social Complexity: Intelligence, Culture, and
Individualized Societies},
Publisher = {HARVARD UNIV PRESS},
Editor = {DeWaal, FBM and Tyack, PL},
Year = {2003},
Month = {January},
ISBN = {0-674-00929-0},
url = {http://gateway.webofknowledge.com/gateway/Gateway.cgi?GWVersion=2&SrcApp=PARTNER_APP&SrcAuth=LinksAMR&KeyUT=WOS:000184645100008&DestLinkType=FullRecord&DestApp=ALL_WOS&UsrCustomerID=47d3190e77e5a3a53558812f597b0b92},
Abstract = {This chapter focuses on the ‘social intelligence’ of
spotted hyenas (Crocuta crocuta), as inferred by the manner
in which they solve daily problems arising from behavioral
interactions. For comparative purposes, we frame our review
in the context of evolutionary models of primate
intelligence. We begin with a presentation of spotted hyena
natural history, underscoring some of this species’
unusual attributes, followed by a discussion of their life
history variables, highlighting certain features shared with
primates. The ensuing commentary on social organization and
behavioral ecology centers on the balance between aggression
and affiliation, and provides an account of various
mechanisms that contribute toward maintaining group
cohesion. Our final discussion of cooperative hunting and
commuting addresses the cognitive implications of elaborate
foraging strategies. Throughout, we consider aspects of the
spotted hyena’s behavioral repertoire that reflect the
complexity of social interaction and the capacity for
individual storage and retrieval of information about a
changing environment. We propose that current hypotheses
relating life history variables, feeding ecology, and social
complexity to the evolution of primate intelligence should
be tested against other taxa in which species display
similar attributes.},
Key = {fds240163}
}
@article{fds172301,
Author = {Drea, C.M. and Wallen, K.},
Title = {Female sexuality and the myth of male control},
Pages = {29-60},
Booktitle = {Evolution, Gender, and Rape},
Publisher = {Cambridge, MA: MIT Press},
Editor = {C.B. Travis},
Year = {2003},
Abstract = {In A Natural History of Rape: Biological Bases of Sexual
Coercion (MIT Press, 2000), Randy Thornhill and Craig T.
Palmer propose that rape has been evolutionarily selected as
an human male mating strategy. Their conceptualization
emphasizes male control of reproduction and ignores the
significant role that females play in reproductive
decisions. Our chapter illustrates the inadequacy of this
male-centric view of reproduction by demonstrating the
female’s active role in controlling sexual behavior,
reflecting not only her own sexuality, but her control over
male sexual behavior. We draw primarily from the primate
literature, but also examine other mammalian species to
illustrate the variety of female control mechanisms. We
begin with a discussion of specialized physical, structural,
and behavioral female ‘barriers’ to forced copulation,
then present examples of more subtle relationships between
mating strategies, social structure, reproductive cycles,
and sexual behavior that emphasize female sexual desire and
mate choice. We argue that even in simians and humans where
forced copulation occurs, it is minimally effective as a
means of reproduction. Last we discuss post copulatory
mechanisms allowing females control of their reproductive
output. We suggest that, through behavioral, structural,
physiological, and social mechanisms, females are vested
with significant sexual control that limits the reproductive
benefits of sexual coercion.},
Key = {fds172301}
}
@article{fds240222,
Author = {Drea, CM and Vignieri, SN and Cunningham, SB and Glickman,
SE},
Title = {Responses to olfactory stimuli in spotted hyenas (Crocuta
crocuta): I. Investigation of environmental odors and the
function of rolling.},
Journal = {Journal of comparative psychology (Washington, D.C. :
1983)},
Volume = {116},
Number = {4},
Pages = {331-341},
Year = {2002},
Month = {December},
ISSN = {0735-7036},
url = {http://www.ncbi.nlm.nih.gov/pubmed/12539928},
Abstract = {Olfaction is crucial to spotted hyenas (Crocuta crocuta),
yet there are no controlled studies of their reactions to
odors. In Experiment 1, the authors examined responses of
captive hyenas to various environmental (prey, nonprey
animal, and plant) odors. Subjects approached and sniffed
all odors equally but preferentially licked prey odors,
scent marked next to odors, and rolled in animal-based
odors. In Experiment 2, the authors examined the function of
rolling by applying odors to the pelts of captive hyenas.
When hyenas wore carrion, they gained positive social
attention (increased investigation and allogrooming) from
pen mates, but when they wore camphor, the normal social
greeting ceremony was curtailed. Thus, olfactory stimuli
elicit specific responses, influence where behavior is
directed, and can be used to affect social
interaction.},
Doi = {10.1037/0735-7036.116.4.331},
Key = {fds240222}
}
@article{fds240220,
Author = {Place, NJ and Holekamp, KE and Sisk, CL and Weldele, ML and Coscia, EM and Drea, CM and Glickman, SE},
Title = {Effects of prenatal treatment with antiandrogens on
luteinizing hormone secretion and sex steroid concentrations
in adult spotted hyenas, Crocuta crocuta.},
Journal = {Biology of reproduction},
Volume = {67},
Number = {5},
Pages = {1405-1413},
Year = {2002},
Month = {November},
ISSN = {0006-3363},
url = {http://www.ncbi.nlm.nih.gov/pubmed/12390869},
Abstract = {Prenatal androgen treatment can alter LH secretion in female
offspring, often with adverse effects on ovulatory function.
However, female spotted hyenas (Crocuta crocuta), renowned
for their highly masculinized genitalia, are naturally
exposed to high androgen levels in utero. To determine
whether LH secretion in spotted hyenas is affected by
prenatal androgens, we treated pregnant hyenas with
antiandrogens (flutamide and finasteride). Later, adult
offspring of the antiandrogen-treated (AA) mothers underwent
a GnRH challenge to identify sex differences in the LH
response and to assess the effects of prenatal antiandrogen
treatment. We further considered the effects of blocking
prenatal androgens on plasma sex steroid concentrations. To
account for potential differences in the reproductive state
of females, we suppressed endogenous hormone levels with a
long-acting GnRH agonist (GnRHa) and then measured plasma
androgens after an hCG challenge. Plasma concentrations of
LH were sexually dimorphic in spotted hyenas, with females
displaying higher levels than males. Prenatal antiandrogen
treatment also significantly altered the LH response to
GnRH. Plasma estradiol concentration was higher in
AA-females, whereas testosterone and androstenedione levels
tended to be lower. This trend toward lower androgen levels
disappeared after GnRHa suppression and hCG challenge. In
males, prenatal antiandrogen treatment had long-lasting
effects on circulating androgens: AA-males had lower T
levels than control males. The sex differences and effects
of prenatal antiandrogens on LH secretion suggest that the
anterior pituitary gland of the female spotted hyena is
partially masculinized by the high androgen levels that
normally occur during development, without adverse effects
on ovulatory function.},
Doi = {10.1095/biolreprod.102.004226},
Key = {fds240220}
}
@article{fds240223,
Author = {Drea, CM and Place, NJ and Weldele, ML and Coscia, EM and Licht, P and Glickman, SE},
Title = {Exposure to naturally circulating androgens during foetal
life incurs direct reproductive costs in female spotted
hyenas, but is prerequisite for male mating.},
Journal = {Proceedings. Biological sciences},
Volume = {269},
Number = {1504},
Pages = {1981-1987},
Year = {2002},
Month = {October},
ISSN = {0962-8452},
url = {http://www.ncbi.nlm.nih.gov/pubmed/12396496},
Keywords = {masculinization; androgen; sexual differentiation;
reproductive success; spotted hyaena},
Abstract = {Among all extant mammals, only the female spotted hyena
(Crocuta crocuta) mates and gives birth through the tip of a
peniform clitoris. Clitoral morphology is modulated by
foetal exposure to endogenous, maternal androgens. First
births through this organ are prolonged and remarkably
difficult, often causing death in neonates. Additionally,
mating poses a mechanical challenge for males, as they must
reach an anterior position on the female's abdomen and then
achieve entry at the site of the retracted clitoris. Here,
we report that interfering with the actions of androgens
prenatally permanently modifies hyena urogenital anatomy,
facilitating subsequent parturition in nulliparous females
who, thereby, produce live cubs. By contrast, comparable,
permanent anatomical changes in males probably preclude
reproduction, as exposure to prenatal anti-androgens
produces a penis that is too short and has the wrong shape
necessary for insertion during copulation. These data
demonstrate that the reproductive costs of clitoral delivery
result from exposure of the female foetus to naturally
circulating androgens. Moreover, the same androgens that
render an extremely unusual and laborious process even more
reproductively costly in the female are apparently essential
to the male's physical ability to reproduce with a normally
masculinized female.},
Doi = {10.1098/rspb.2002.2109},
Key = {fds240223}
}
@article{fds240176,
Author = {Place, NJ and Holekamp, KE and Sisk, CL and Weldele, ML and Coscia, EM and Drea, CM and Glickman, SE},
Title = {Persistent effects of prenatal treatment with anti-androgens
on the hypothalamic-pituitary-gonadal axis of adult spotted
hyenas.},
Journal = {BIOLOGY OF REPRODUCTION},
Volume = {66},
Series = {Paper presented at the 35th Annual Meeting of the Society
for the Study of Reproduction, Baltimore,
MD},
Pages = {306-306},
Publisher = {SOC STUDY REPRODUCTION},
Year = {2002},
Month = {January},
ISSN = {0006-3363},
url = {http://gateway.webofknowledge.com/gateway/Gateway.cgi?GWVersion=2&SrcApp=PARTNER_APP&SrcAuth=LinksAMR&KeyUT=WOS:000176561900572&DestLinkType=FullRecord&DestApp=ALL_WOS&UsrCustomerID=47d3190e77e5a3a53558812f597b0b92},
Key = {fds240176}
}
@article{fds240221,
Author = {Drea, CM and Vignieri, SN and Kim, HS and Weldele, ML and Glickman,
SE},
Title = {Responses to olfactory stimuli in spotted hyenas (Crocuta
crocuta): II. Discrimination of conspecific
scent},
Journal = {Journal of Comparative Psychology},
Volume = {116},
Number = {4},
Pages = {342-349},
Year = {2002},
ISSN = {0735-7036},
url = {http://www.ncbi.nlm.nih.gov/pubmed/12539929},
Abstract = {Scent marking in spotted hyenas (Crocuta crocuta) includes
the deposition of anal sac secretions, or “paste,” and
presumably advertises territorial ownership. To test whether
captive hyenas classify and discriminate individuals using
odor cues in paste, the authors conducted behavioral
discrimination bioassays and recorded hyena investigation of
paste extracted from various conspecific donors. In
Experiment 1, subjects directed most investigative behavior
toward scents from unfamiliar hyenas and members of the
opposite sex. In Experiment 2, male hyenas discriminated
between concurrent presentations of paste from various
unfamiliar females in similar reproductive state. Thus,
pasted scent marks convey information about the sex,
familiarity, and even identity of conspecifics. Aside from
territory maintenance, scent marking may also communicate
information about individual sexual status.},
Doi = {10.1037//0735-7036.116.4.342},
Key = {fds240221}
}
@article{fds240173,
Author = {Place, NJ and Drea, CM and Holekamp, KE and Weldele, ML and Coscia, EM and Glickman, SE},
Title = {Sex differences and effects of prenatal anti-androgens on LH
secretion in spotted hyenas.},
Journal = {AMERICAN ZOOLOGIST},
Volume = {41},
Number = {6},
Pages = {1557-1557},
Publisher = {SOC INTEGRATIVE COMPARATIVE BIOLOGY},
Year = {2001},
Month = {December},
ISSN = {0003-1569},
url = {http://gateway.webofknowledge.com/gateway/Gateway.cgi?GWVersion=2&SrcApp=PARTNER_APP&SrcAuth=LinksAMR&KeyUT=WOS:000174306500611&DestLinkType=FullRecord&DestApp=ALL_WOS&UsrCustomerID=47d3190e77e5a3a53558812f597b0b92},
Key = {fds240173}
}
@article{fds240186,
Author = {Drea, CM and Wallen, K},
Title = {Low-status monkeys "play dumb" when learning in mixed social
groups.},
Journal = {Proceedings of the National Academy of Sciences of the
United States of America},
Volume = {96},
Series = {Proceedings of the National Academy of Sciences,
USA},
Number = {22},
Pages = {12965-12969},
Year = {1999},
Month = {October},
ISSN = {0027-8424},
url = {http://www.ncbi.nlm.nih.gov/pubmed/10536031},
Abstract = {Many primates, including humans, live in complex
hierarchical societies where social context and status
affect daily life. Nevertheless, primate learning studies
typically test single animals in limited laboratory settings
where the important effects of social interactions and
relationships cannot be studied. To investigate the impact
of sociality on associative learning, we compared the
individual performances of group-tested rhesus monkeys
(Macaca mulatta) across various social contexts. We used a
traditional discrimination paradigm that measures an
animal's ability to form associations between cues and the
obtaining of food in choice situations; but we adapted the
task for group testing. After training a 55-member colony to
separate on command into two subgroups, composed of either
high- or low-status families, we exposed animals to two
color discrimination problems, one with all monkeys present
(combined condition), the other in their "dominant" and
"subordinate" cohorts (split condition). Next, we
manipulated learning history by testing animals on the same
problems, but with the social contexts reversed. Monkeys
from dominant families excelled in all conditions, but
subordinates performed well in the split condition only,
regardless of learning history. Subordinate animals had
learned the associations, but expressed their knowledge only
when segregated from higher-ranking animals. Because
aggressive behavior was rare, performance deficits probably
reflected voluntary inhibition. This experimental evidence
of rank-related, social modulation of performance calls for
greater consideration of social factors when assessing
learning and may also have relevance for the evaluation of
human scholastic achievement.},
Doi = {10.1073/pnas.96.22.12965},
Key = {fds240186}
}
@article{fds240229,
Author = {Drea, CM},
Title = {Status, age, and sex effects on performance of
discrimination tasks in group-tested rhesus monkeys (Macaca
mulatta).},
Journal = {Journal of comparative psychology (Washington, D.C. :
1983)},
Volume = {112},
Number = {2},
Pages = {170-182},
Year = {1998},
Month = {June},
ISSN = {0735-7036},
url = {http://www.ncbi.nlm.nih.gov/pubmed/9642786},
Abstract = {To assess the relation between performance and social or
demographic variables, this study group tested a captive
monkey colony on visual and manual discrimination problems.
Animals could choose between differently colored,
sand-filled boxes, where hue signaled the initial
probability of finding buried food items. Dominant animals
and subadults were most successful in locating and
retrieving incentives, but sex did not affect performance.
Rank effects occurred without overt aggression, suggesting
deference by subordinates as a mediating mechanism. Age
effects may reflect changing attention patterns only evident
in complex arenas where cue salience becomes diluted.
Because these findings differ from studies of singly tested
animals, they show that, in a social context, an
individual's rank and age may define opportunities to gain
or efficiently use information.},
Doi = {10.1037/0735-7036.112.2.170},
Key = {fds240229}
}
@article{fds240217,
Author = {Glickman, SE and Coscia, EM and Frank, LG and Licht, P and Weldele, ML and Drea, CM},
Title = {Androgens and masculinization of genitalia in the spotted
hyaena (Crocuta crocuta). 3. Effects of juvenile
gonadectomy.},
Journal = {Journal of reproduction and fertility},
Volume = {113},
Number = {1},
Pages = {129-135},
Year = {1998},
Month = {May},
ISSN = {0022-4251},
url = {http://www.ncbi.nlm.nih.gov/pubmed/9713385},
Keywords = {castration • ovariectomy • development •
hyaena},
Abstract = {Studies involving the administration of anti-androgens to
spotted hyaenas during fetal development have raised
questions concerning the precise contributions of steroids
to phallic growth in these animals. If gonadal androgens
promote postnatal penile growth in males, the following
would be expected: (a) a period of accelerated growth
accompanying achievement of puberty, and (b) a marked
reduction in adult penile size and density of penile spines
after gonadectomy. If a similar androgenic pubertal process
stimulates clitoral growth in these highly 'masculinized'
hyaenas, parallel observations in females would be expected;
however, the role of oestrogens in accounting for
female-typical clitoral development would also have to be
considered. The results of the present study suggest a
limited role, if any for androgenic stimulation of phallic
growth. That is, penile growth was greater during the 10
month period preceding puberty, than during an 18-month
period that included the traditional increase in pubertal
androgens. In addition, pre-pubertal castration had minimal
effects on penile length, diameter, or the presence of
penile spines. In females, most clitoral growth also
occurred before puberty, although pre-pubertal ovariectomy
produced significant reductions in clitoral diameter and the
elasticity of the urogenital meatus. These feminine
characteristics which normally distinguish the female from
the male phallus in this species, were partially restored by
a brief period of oestrogen administration. Both sexes
displayed erections many years after pre-pubertal
castration. The results of the present study suggest that
postnatal phallic growth is largely independent of gonadal
steroids, with oestrogenic facilitation of female-typical
clitoral characteristics in spotted hyaenas.},
Doi = {10.1530/jrf.0.1130129},
Key = {fds240217}
}
@article{fds240218,
Author = {Drea, CM and Weldele, ML and Forger, NG and Coscia, EM and Frank, LG and Licht, P and Glickman, SE},
Title = {Androgens and masculinization of genitalia in the spotted
hyaena (Crocuta crocuta). 2. Effects of prenatal
anti-androgens.},
Journal = {Journal of reproduction and fertility},
Volume = {113},
Number = {1},
Pages = {117-127},
Year = {1998},
Month = {May},
ISSN = {0022-4251},
url = {http://www.ncbi.nlm.nih.gov/pubmed/9713384},
Keywords = {anti-androgen • masculinization • feminization
• development • hyaena},
Abstract = {Pregnant spotted hyaenas were treated with anti-androgens to
interfere with the unusually masculine 'phallic' development
that characterizes females of this species. The effects on
genital morphology and plasma androgen concentrations of
infants were studied during the first 6 months of life.
Although there were consistent 'feminizing' effects of
prenatal anti-androgen treatment on genital morphology in
both sexes, such exposure did not produce males with extreme
hypospadia, as it does in other species, nor did it produce
females with a 'typical' mammalian clitoris and external
vagina. 'Feminization' of males resulted in a penis with the
morphological features of the hyaena clitoris, and
'feminization' of females exaggerated the sex differences
that are typical of this species. The effects of treatment
were present at birth and persisted for at least 6 months.
Treatment of pregnant females with flutamide and finasteride
also markedly reduced circulating concentrations of
testosterone and dihydrotestosterone in maternal plasma
during pregnancy. Plasma delta 4-androstenedione was reduced
in the female, but not the male, infants of treated mothers,
consistent with an epigenetic hypothesis previously advanced
to explain hormonal 'masculinization' of females. The
present 'feminizing' effects of prenatal anti-androgen
treatment are consistent with contemporary understanding of
sexual differentiation, which accounts for morphological
variation between the sexes in terms of steroids. However,
current theory does not account for the basic genital
structure of females and the present data suggest that
development of the male penis and scrotum, and the female
clitoris and pseudoscrotum, in spotted hyaenas may involve
both androgen-dependent and androgen-independent
components.},
Doi = {10.1530/jrf.0.1130117},
Key = {fds240218}
}
@article{fds304455,
Author = {Drea, CM},
Title = {Social context affects how rhesus monkeys explore their
environment.},
Journal = {American journal of primatology},
Volume = {44},
Number = {3},
Pages = {205-214},
Year = {1998},
Month = {January},
ISSN = {0275-2565},
url = {http://www.ncbi.nlm.nih.gov/pubmed/9519240},
Abstract = {This study reports on social modulation of exploratory
behavior and response to novelty by members of a captive
rhesus monkey colony. The group was trained to split in
half, with one subgroup composed of dominant members only,
the other of subordinates. The animals were then presented
the same initially novel stimuli (i.e., sand-filled metal
boxes containing hidden food items) in two social contexts
differing in hierarchical composition. In a combined
context, all group members (i.e., both subgroups together)
were simultaneously presented the stimuli. In a split
context, only members of the top or bottom half of the group
(i.e., each subgroup in turn) was independently presented
the stimuli. Subordinates responded similarly to dominant
animals in the combined context but differently in the split
context, where they were far more hesitant. Rank-related
differences were evident in the way animals used their home
compound and in their approach and responsiveness toward the
stimuli. These findings show that social context influences
how animals explore novel situations, possibly reflecting
different social roles or status effects on the perception
of social structure. Also, despite the complexity of primate
social relationships, the separation technique produced no
permanent or adverse effects on the social integrity of the
group. This study shows that manipulating the social
environment through separation training can be a powerful
tool for assessing contextual influences on
behavior.},
Doi = {10.1002/(sici)1098-2345(1998)44:3<205::aid-ajp3>3.0.co;2-#},
Key = {fds304455}
}
@article{fds240219,
Author = {Drea, CM},
Title = {Social context affects how rhesus monkeys explore their
environment},
Journal = {American Journal of Primatology},
Volume = {44},
Number = {3},
Pages = {205-214},
Publisher = {WILEY},
Year = {1998},
ISSN = {0275-2565},
url = {http://www.ncbi.nlm.nih.gov/pubmed/9519240},
Keywords = {exploration • response to novelty • rhesus monkeys
• social roles • social context • dominance
relationships},
Abstract = {This study reports on social modulation of exploratory
behavior and response to novelty by members of a captive
rhesus monkey colony. The group was trained to split in
half, with one subgroup composed of dominant members only,
the other of subordinates. The animals were then presented
the same initially novel stimuli (i.e., sand-filled metal
boxes containing hidden food items) in two social contexts,
differing in hierarchical composition. In a ‘combined’
context, all group members (i.e., both subgroups together)
were simultaneously presented the stimuli. In a ‘split’
context, only members of the top or bottom half of the group
(i.e., each subgroup in turn) was independently presented
the stimuli. Subordinates responded similarly to dominant
animals in the combined context, but differently in the
split context, where they were far more hesitant.
Rank-related differences were evident in the way animals
used their home compound and in their approach and
responsiveness toward the stimuli. These findings show that
social context influences how animals explore novel
situations, possibly reflecting different social roles or
status effects on the perception of social structure. Also,
despite the complexity of primate social relationships, the
separation technique produced no permanent or adverse
effects on the social integrity of the group. This study
shows that manipulating the social environment through
separation training can be a powerful tool for assessing
contextual influences on behavior.},
Doi = {10.1002/(SICI)1098-2345(1998)44:33.0.CO;2},
Key = {fds240219}
}
@article{fds240183,
Author = {Glickman, SE and Zabel, CJ and Yoerg, SI and Weldele, ML and Drea, CM and Frank, LG},
Title = {Social facilitation, affiliation, and dominance in the
social life of spotted hyenas.},
Journal = {Annals of the New York Academy of Sciences},
Volume = {807},
Series = {Annals of the New York Academy of Sciences, Vol. 807: The
Integrative Neurobiology of Affiliation},
Pages = {175-184},
Publisher = {NY: New York Academy of Sciences},
Editor = {C.S. Carter and I. I. Lederhendler and B. Kirkpatrick},
Year = {1997},
Month = {January},
ISSN = {0077-8923},
url = {http://www.ncbi.nlm.nih.gov/pubmed/9071350},
Doi = {10.1111/j.1749-6632.1997.tb51919.x},
Key = {fds240183}
}
@article{fds240184,
Author = {Drea, CM and Hawk, JE and Glickman, SE},
Title = {The emergence of affiliative behavior in infant spotted
hyenas (Crocuta crocuta).},
Journal = {Annals of the New York Academy of Sciences},
Volume = {807},
Series = {Annals of the New York Academy of Sciences, Vol. 807: The
Integrative Neurobiology of Affiliation},
Pages = {498-500},
Publisher = {NY: New York Academy of Sciences},
Editor = {C.S. Carter and I.I. Lederhendler and B. Kirkpatrick},
Year = {1997},
Month = {January},
ISSN = {0077-8923},
url = {http://www.ncbi.nlm.nih.gov/pubmed/9071381},
Doi = {10.1111/j.1749-6632.1997.tb51950.x},
Key = {fds240184}
}
@article{fds240171,
Author = {Drea, CM},
Title = {Primate Handedness: An Emerging Discipline?},
Journal = {Contemporary Psychology: A Journal of Reviews},
Volume = {41},
Number = {7},
Pages = {681-682},
Publisher = {Portico},
Year = {1996},
Month = {July},
ISSN = {0010-7549},
url = {http://gateway.webofknowledge.com/gateway/Gateway.cgi?GWVersion=2&SrcApp=PARTNER_APP&SrcAuth=LinksAMR&KeyUT=WOS:A1996UW96500026&DestLinkType=FullRecord&DestApp=ALL_WOS&UsrCustomerID=47d3190e77e5a3a53558812f597b0b92},
Doi = {10.1037/004622},
Key = {fds240171}
}
@article{fds240182,
Author = {Drea, CM and Hawk, JE and Glickman, SE},
Title = {Aggression decreases as play emerges in infant spotted
hyaenas: Preparation for joining the clan},
Journal = {Animal Behaviour},
Volume = {51},
Number = {6},
Pages = {1323-1336},
Publisher = {Elsevier BV},
Year = {1996},
Month = {January},
url = {http://dx.doi.org/10.1006/anbe.1996.0136},
Abstract = {The early social development of spotted hyaenas, Crocuta
crocuta, is marked by a dramatic transition at 2-3 weeks of
age, when infants are taken from the isolation of their
natal den, where they are intensely aggressive, to the
communal den, where they meet most clan members for the
first time. This study examined behaviour patterns in eight
sets of captive twins during the first month of life to
document the changes that prepare young hyaenas for social
integration at the communal den. Bite shakes, the most
extreme aggressive behaviour, declined markedly within the
first week of life, but other forms of aggression remained
constant. During week 1, low- intensity prosocial behaviour
occurred primarily between mother and cub. By week 2,
higher-intensity social play emerged, occurring mainly
between siblings. In weeks 3 and 4, cub interactive play was
most frequent, lasted longer and was more vigorous.
Locomotor and object play did not emerge until weeks 3 and
4, respectively. Dominance relations between siblings were
operationally defined by submissive withdrawals.
Accordingly, aggression was unidirectional, with dominants
initiating most interactions. By contrast, play was
reciprocal and equally initiated by dominant and subordinate
cubs. Maternal interruption of cub behaviour mainly occurred
during extreme aggressive interactions, but rarely during
vigorous play. Results showed that prosocial behaviour
emerged in captive hyaena cubs following a decline in severe
aggression and before the time wild cubs are taken from the
natal to the communal den. It is suggested that play may
modulate aggression, following the establishment of a
dominance relationship, and may serve an immediate prosocial
function to prepare aggressive infant hyaenas for
integration into the clan.},
Doi = {10.1006/anbe.1996.0136},
Key = {fds240182}
}
@article{fds240215,
Author = {Drea, CM and Wallen, K and Akinbami, MA and Mann,
DR},
Title = {Neonatal testosterone and handedness in yearling rhesus
monkeys (Macaca mulatta).},
Journal = {Physiology & behavior},
Volume = {58},
Number = {6},
Pages = {1257-1262},
Year = {1995},
Month = {December},
ISSN = {0031-9384},
url = {http://www.ncbi.nlm.nih.gov/pubmed/8623029},
Keywords = {Cerebral laterality • Handedness • Neonatal
testosterone • Rhesus monkey • GnRH antagonist
• Androgen suppression • Social
environment},
Abstract = {This study investigated the relationship between neonatal
testosterone (T) and hand bias in young rhesus monkeys
(Macaca mulatta). Subjects (n = 8 per group) included:
neonatally androgen-suppressed males, using a Nal-Lys
gonadotropin releasing hormone (GnRH) antagonist (Antide);
androgen-suppressed males receiving T replacement by a
long-acting T preparation (CDB); control males; and control
females. Antide suppressed T to the female range, whereas
CDB replacement produced supranormal levels. Visually guided
reaching, in a social context, showed a population-level
left-hand bias. Males with elevated T did not show a
stronger left-hand bias than males with normal T, but did
show a stronger bias for the preferred hand whether left or
right. Males with Antide-suppressed T showed an intermediate
degree of hand bias. Results suggest that high neonatal T
levels affect laterality and raise the possibility that GnRH
analogues influence brain development. These data suggest a
broad influence of the CNS-pituitary-testicular axis on
brain asymmetries and provide support for an early neonatal
period of T-influenced brain differentiation.},
Doi = {10.1016/0031-9384(95)02026-8},
Key = {fds240215}
}
@article{fds240216,
Author = {Drea, CM and Wallen, K},
Title = {Gradual acquisition of visual discrimination tasks in a
social group of rhesus monkeys (Macaca mulatta)},
Journal = {Animal Learning & Behavior},
Volume = {23},
Number = {1},
Pages = {1-8},
Publisher = {Springer Nature},
Year = {1995},
Month = {March},
ISSN = {0090-4996},
url = {http://dx.doi.org/10.3758/BF03198009},
Abstract = {An established, captive colony of 74 rhesus monkeys (Macaca
mulatta) was group-tested on a simultaneous visual
discrimination problem and three reversals of the initial
discrimination. The task incorporated important aspects of
rhesus foraging behavior. Although other studies of communal
groups of nonhuman primates have reported rapid learning,
subjects in the present study showed no evidence of
one-trial acquisition of the initial problem or of rapid
learning-set formation across the reversal series. Instead,
mean and individual performance, on all variables measured,
improved gradually, both within and across series. Subjects
appeared to "learn how to learn," consistent with findings
of traditional studies of individual discrimination
learning. Our finding of gradual learning in group-living
animals argues that the source of rapid learning in previous
reports is not attributable to social influence or
ecological relevance, but may reflect specific procedural or
species differences between studies. © 1995 Psychonomic
Society, Inc.},
Doi = {10.3758/BF03198009},
Key = {fds240216}
}
@article{fds44333,
Author = {Drea, C.M.},
Title = {Influence of social dominance on the acquisition of color
discriminations in rhesus monkeys (Macaca
mulatta)},
Series = {Ph.D. Thesis, Emory University, Atlanta, GA. 130
pages},
Year = {1991},
Key = {fds44333}
}
@article{fds240214,
Author = {Fagot, J and Drea, CM and Wallen, K},
Title = {Asymmetrical hand use in rhesus monkeys (Macaca mulatta) in
tactually and visually regulated tasks.},
Journal = {Journal of comparative psychology (Washington, D.C. :
1983)},
Volume = {105},
Number = {3},
Pages = {260-268},
Year = {1991},
ISSN = {0735-7036},
url = {http://www.ncbi.nlm.nih.gov/pubmed/1935005},
Abstract = {Asymmetrical hand use by rhesus monkeys (Macaca mulatta) was
investigated in a series of tactually and visually guided
tasks. The 1st experiment recorded manual preferences of 29
monkeys for solving a haptic discrimination task in a
hanging posture. There was a left-hand population bias: 21
monkeys had a left-hand bias, 4 a right-hand bias, and 4 no
bias. The 2nd experiment, 4 tasks with 23 to 51 monkeys,
investigated the critical components of the 1st experiment
by varying the posture (hanging, sitting, or tripedal) and
the sensory requirements (tactile or visual). Posture
influenced hand bias, with a population-level left-hand bias
in hanging and sitting postures, but an almost symmetrical
distribution in the tripedal posture. A left-hand bias was
found for both sensory modalities, but the bias was stronger
in the tactual tasks. Results suggest a possible
right-hemisphere specialization in the rhesus for tactile,
visual, or spatial processing.},
Doi = {10.1037//0735-7036.105.3.260},
Key = {fds240214}
}
@article{fds44332,
Author = {Drea, C.M.},
Title = {). Influence of social factors on discrimination learning
and the acquisition of a reversal learning set in rhesus
monkeys (Macaca mulatta)},
Series = {M.A. Thesis, Emory University, Atlanta, GA. 119
pages},
Year = {1990},
Key = {fds44332}
}
@article{fds240213,
Author = {Nagata, M and Hohman, TC and Nishimura, C and Drea, CM and Oliver, C and Robison, WG},
Title = {Polyol and vacuole formation in cultured canine lens
epithelial cells.},
Journal = {Experimental eye research},
Volume = {48},
Number = {5},
Pages = {667-677},
Year = {1989},
Month = {May},
ISSN = {0014-4835},
url = {http://www.ncbi.nlm.nih.gov/pubmed/2500357},
Abstract = {Polyol accumulation and myo-inositol depletion were
accompanied by extensive vacuole formation in cultured
canine lens epithelial cells that were incubated for up to
96 hr in growth medium supplemented with 30 mM D-galactose
or 30 mM D-glucose. These changes did not occur in cells
incubated in a hypergalactosemic or hyperglycemic medium
which also contained an aldose reductase inhibitor (20
microM sorbinil). In addition, these changes were not
observed in lens cells incubated in growth medium
supplemented with either 30 mM mannitol, which is known to
enter cells only slowly, or in 30 mM L-galactose, which is
not a substrate for aldose reductase. The vacuoles were
visible at the ultrastructural level after 6 hr of
incubation in 30 mM D-galactose and increased in both number
and size with time. These vacuoles had a unique fine
structure. They did not result from swelling of mitochondria
or other cell organelles. As demonstrated cytochemically,
they did not represent either lysosomes or Golgi saccules.
The proliferation pattern of cells incubated with 30 mM
D-galactose was clearly different from that of control
cells, but approached normal when an aldose reductase
inhibitor was added to the incubation medium. Together these
findings suggest that vacuole formation and altered cell
proliferation were caused by polyol accumulation and/or
myo-inositol loss, both of which result from aldose
reductase activity.},
Doi = {10.1016/0014-4835(89)90008-0},
Key = {fds240213}
}
@article{fds240211,
Author = {Katz, ML and Drea, CM and Robison, WG},
Title = {Dietary vitamins A and E influence retinyl ester composition
and content of the retinal pigment epithelium.},
Journal = {Biochimica et biophysica acta},
Volume = {924},
Number = {3},
Pages = {432-441},
Year = {1987},
Month = {June},
ISSN = {0006-3002},
url = {http://www.ncbi.nlm.nih.gov/pubmed/3593761},
Abstract = {Experiments were conducted to determine the influence of
dietary levels of vitamin A and alpha-tocopherol on the
amounts and composition of retinyl esters in the retinal
pigment epithelium of light-adapted albino rats. Groups of
rats were fed diets containing alpha-tocopherol and either
no retinyl palmitate, adequate retinyl palmitate, or
excessive retinyl palmitate. Other groups of rats received
diets lacking alpha-tocopherol and containing the same three
levels of retinyl palmitate. Retinoic acid was added to
diets lacking retinyl palmitate. After 27 weeks, the animals
were light-adapted to achieve essentially total visual
pigment bleaches, and the neural retinas and retinal pigment
epithelium-eyecups were then dissected from each eye for
vitamin A ester determinations. Almost all of the retinyl
esters were found in the retinal pigment epithelium-eyecup
portions of the eyes, mainly as retinyl palmitate and
retinyl stearate. Maintaining rats on a vitamin A-deficient,
retinoic acid-containing diet led to significant reductions
in retinal pigment epithelial retinyl ester levels in rats
fed both the vitamin E-supplemented and vitamin E-deficient
diets; contrary to expectations, the effect of dietary
vitamin A deficiency was more pronounced in the vitamin
E-supplemented rats. Vitamin A deficiency in retinoic
acid-maintained animals also led to significant reductions
in retinyl palmitate-to-stearate ester ratios in the retinal
pigment epithelia of both vitamin E-supplemented and vitamin
E-deficient rats. Excessive dietary intake of vitamin A had
little, if any, effect on retinal pigment epithelial retinyl
ester content or composition. Vitamin E deficiency resulted
in significant increases in retinal pigment epithelial
retinyl palmitate content and in palmitate-to-stearate ester
ratios in rats fed all three levels of vitamin A, but had
little effect on retinal pigment epithelial retinyl stearate
content. In other tissues, vitamin E deficiency has been
shown to lower vitamin A levels, and it is widely accepted
that this effect is due to autoxidative destruction of
vitamin A. The increase in retinal pigment epithelial
vitamin A ester levels in response to vitamin E deficiency
indicates that vitamin E does not regulate vitamin A levels
in this tissue primarily by acting as an antioxidant, but
rather may act as an inhibitor of vitamin A uptake and/or
storage. The effect of vitamin E on pigment epithelial
vitamin A levels may be mediated by the vitamin E-induced
change in retinyl palmitate-to-stearate ratios.},
Doi = {10.1016/0304-4165(87)90157-7},
Key = {fds240211}
}
@article{fds240212,
Author = {Katz, ML and Drea, CM and Robison, WG},
Title = {Age-related alterations in vitamin A metabolism in the rat
retina.},
Journal = {Experimental eye research},
Volume = {44},
Number = {6},
Pages = {939-949},
Year = {1987},
Month = {June},
ISSN = {0014-4835},
url = {http://www.ncbi.nlm.nih.gov/pubmed/3653281},
Abstract = {Vitamin A plays a central role in visual transduction and in
maintaining the structural integrity of the retina. It is
possible that age-related alterations in vitamin A
metabolism in the eye could contribute to the impairment of
visual function that occurs during senescence. Therefore,
investigations were conducted to determine whether the
metabolism of this vitamin in the rat retina was altered
during aging. Pigmented rats aged 12-, 22-, and 32 months
were dark-adapted, and one eye from each animal was
enucleated under dim red light. The neural retinas were
separated from the retinal pigment epithelium
(RPE)-choroid-scleral complexes, and the amounts and forms
of vitamin A in both tissues were determined. The animals
were then fully light-adapted, and the same measurements
were performed on the tissues from the remaining eye of each
rat. A number of age-related alterations in the vitamin A
composition and content of the retina and RPE were observed.
The most pronounced of these changes were significant
increases in the ratios of retinyl palmitate to retinyl
stearate with advancing age in both the neural retina and
RPE. The total vitamin A ester contents of the RPEs
increased during senescence in the dark-adapted state, but
not in the light-adapted state. Retinyl ester levels in the
neural retinas, on the other hand, did not differ
significantly between 12- and 32-month-old animals in either
the light-adapted or dark-adapted states. The amounts of
all-trans retinol in the neural retinas decreased during
aging, mainly in the dark-adapted state, whereas aging had
no influence on RPE all-trans retinol content. The
age-related alterations in metabolism of vitamin A that
these observations reflect may be related to certain changes
in visual function that occur during senescence.},
Doi = {10.1016/s0014-4835(87)80055-6},
Key = {fds240212}
}
@article{fds44338,
Author = {Katz, M.L. and Robison, W. G., Jr. and Drea,
C.M.},
Title = {Factors influencing lipofuscin accumulation in the retinal
pigment epithelium of the eye},
Series = {Advances in the Biosciences, Vol. 64: Advances in Age
Pigments Research},
Pages = {111-132},
Publisher = {Oxford: Pergamon Press},
Editor = {E.A. Totaro and P.N. Glees and F.A. Pisanti},
Year = {1987},
Key = {fds44338}
}
@article{fds240209,
Author = {Katz, ML and Drea, CM and Eldred, GE and Hess, HH and Robison,
WG},
Title = {Influence of early photoreceptor degeneration on lipofuscin
in the retinal pigment epithelium.},
Journal = {Experimental eye research},
Volume = {43},
Number = {4},
Pages = {561-573},
Year = {1986},
Month = {October},
ISSN = {0014-4835},
url = {http://www.ncbi.nlm.nih.gov/pubmed/3792460},
Abstract = {Experiments were conducted to evaluate the role played by
photoreceptor cells in the accumulation of age pigment, or
lipofuscin, in the retinal pigment epithelium (RPE). The
age-related accumulation of RPE lipofuscin was compared
between rats with hereditary photoreceptor degeneration
(RDY) and congenic rats with normal retinas. In the RDY
animals, the age-related increase in RPE lipofuscin content
was substantially less than in normal controls. This
suggests that the photoreceptor cells play a significant
role in RPE lipofuscin deposition, although they may not be
the sole contributors to RPE lipofuscin formation. Evidence
that outer-segment components may be converted into
lipofuscin fluorophores was provided by the discovery that
in young RDY rats, fragments of outer segments from
degenerating photoreceptor cells had fluorescence properties
similar to those of RPE lipofuscin. Chloroform-methanol
extraction of retina-RPE tissue from young normal and
dystrophic rats, and analysis of the chloroform fractions by
thin-layer chromatography, revealed three distinct
fluorescent components associated with the lipofuscin-like
fluorescence of the outer-segment fragments in the RDY
rats.},
Doi = {10.1016/s0014-4835(86)80023-9},
Key = {fds240209}
}
@article{fds240210,
Author = {Katz, ML and Drea, CM and Robison, WG},
Title = {Relationship between dietary retinol and lipofuscin in the
retinal pigment epithelium.},
Journal = {Mechanisms of ageing and development},
Volume = {35},
Number = {3},
Pages = {291-305},
Year = {1986},
Month = {August},
ISSN = {0047-6374},
url = {http://www.ncbi.nlm.nih.gov/pubmed/3773574},
Abstract = {A variety of evidence suggests that autoxidation of cellular
components probably plays a significant role in the
age-related accumulation of lipofuscin, or age-pigment, in
the mammalian retinal pigment epithelium (RPE). Among the
likely candidates for conversion into RPE lipofuscin
fluorophores via autoxidative mechanisms are vitamin A
compounds, which are present in the retina and RPE in high
concentrations. Vitamin E, an important lipid antioxidant,
is likely to inhibit vitamin A autoxidation. Experiments
were conducted to evaluate the significance of vitamin A
autoxidation in the deposition of lipofuscin in the RPE.
Albino rats were fed diets either supplemented with or
lacking vitamin E. Each of these two groups of animals was
further subdivided into three groups which were fed
different levels of vitamin A palmitate: none, 14.0 mumol/kg
diet, and 80.5 mumol/kg diet. After 26 weeks, the animals
were killed and the RPE lipofuscin contents were determined
by both fluorescence measurements and quantitative
ultrastructural morphometry. Vitamin A palmitate deficiency
led to significant reductions in RPE lipofuscin deposition,
relative to the amounts of this pigment present in the
groups receiving vitamin A palmitate in their diets. The
relative magnitude of the vitamin A effect was greater in
the vitamin E-supplemented groups than in the groups fed the
diets deficient in vitamin E. This finding suggests that
vitamin E interacts with vitamin A ester metabolites in vivo
in a more complex manner than simply acting as an
antioxidant protectant. Rats fed the diets containing the
higher level of vitamin A palmitate failed to display
elevated RPE lipofuscin contents relative to those in the
rats fed 14.0 mumol of vitamin A palmitate/kg diet. Failure
of high vitamin A intake to enhance RPE lipofuscin
deposition may have been due to the fact that intake of
vitamin A above normal levels did not lead to an elevation
in vitamin A content of the retinal tissue. Establishing an
effect of vitamin A deficiency on RPE lipofuscin deposition
and characterization of the interactions between vitamins E
and A are important steps toward defining precisely the
molecular and cellular mechanisms underlying age-pigment
accumulation in the RPE.},
Doi = {10.1016/0047-6374(86)90131-4},
Key = {fds240210}
}
@article{fds240164,
Author = {DREA, CM and KATZ, ML and ROBISON, WG and HESS, HH},
Title = {INFLUENCE OF EARLY PHOTORECEPTOR DEGENERATION ON LIPOFUSCIN
IN THE RETINAL-PIGMENT EPITHELIUM},
Journal = {AGE},
Volume = {8},
Number = {4},
Pages = {146-146},
Publisher = {AMER AGING ASSOC},
Year = {1985},
Month = {January},
ISSN = {0161-9152},
url = {http://gateway.webofknowledge.com/gateway/Gateway.cgi?GWVersion=2&SrcApp=PARTNER_APP&SrcAuth=LinksAMR&KeyUT=WOS:A1985ATH6500042&DestLinkType=FullRecord&DestApp=ALL_WOS&UsrCustomerID=47d3190e77e5a3a53558812f597b0b92},
Key = {fds240164}
}
@article{fds240179,
Author = {KATZ, ML and DREA, CM and ROBISON, WG},
Title = {RELATIONSHIP BETWEEN DIETARY RETINOL AND LIPOFUSCIN IN THE
RETINAL-PIGMENT EPITHELIUM},
Journal = {AGE},
Volume = {8},
Series = {Poster presented at the 14th Annual Meeting of the American
Aging Association},
Number = {4},
Pages = {145-145},
Publisher = {AMER AGING ASSOC},
Year = {1985},
Month = {January},
ISSN = {0161-9152},
url = {http://gateway.webofknowledge.com/gateway/Gateway.cgi?GWVersion=2&SrcApp=PARTNER_APP&SrcAuth=LinksAMR&KeyUT=WOS:A1985ATH6500041&DestLinkType=FullRecord&DestApp=ALL_WOS&UsrCustomerID=47d3190e77e5a3a53558812f597b0b92},
Key = {fds240179}
}
%% Book Chapters
@misc{fds372419,
Author = {Drea, CM and Tang-Martinez, Z},
Title = {Stephen E. Glickman},
Pages = {141-156},
Booktitle = {Biographical History of Behavioral Neuroendocrinology},
Year = {2022},
Month = {November},
ISBN = {9783031129698},
url = {http://dx.doi.org/10.1007/978-3-031-12970-4_16},
Abstract = {Stephen E. Glickman (1933-2020) was an American comparative
psychologist and scholar of the history of psychology, who
contributed over 100 publications relevant to the study of
animal behavior, cognitive and behavioral neuroscience,
reproductive neuroendocrinology and anatomy, and integrative
and evolutionary biology. His early research career,
spanning roughly 26 years, was dominated by investigation of
the neurological substrates of learning and arousal, and by
the comparative study of curiosity. In his later research
career, spanning roughly 36 years, Glickman was best known
for his illuminating work on the sexual differentiation and
development of the spotted hyena (Crocuta crocuta) - a
species that came to be renowned for the female's highly
unusual suite of 'masculinized' traits. Glickman can be
credited with unraveling many of this species' mysteries,
including by establishing, at the University of California,
Berkeley, the only captive hyena colony worldwide and
assembling a team of highly specialized collaborators who
provided unparalleled research synergy. In honor of his
scientific contributions and the creation of this unique
intellectual environment, the field station of UC Berkeley
was renamed, in 2020, the "Stephen Glickman Field Station
for the Study of Behavior, Ecology and Reproduction."},
Doi = {10.1007/978-3-031-12970-4_16},
Key = {fds372419}
}
@misc{fds367218,
Author = {Drea, CM and Grebe, NM},
Title = {Intraspecific aggression and social dominance},
Pages = {160-174},
Booktitle = {The Routledge International Handbook of Comparative
Psychology},
Year = {2022},
Month = {September},
ISBN = {9780367546045},
url = {http://dx.doi.org/10.4324/9781003091868-16},
Doi = {10.4324/9781003091868-16},
Key = {fds367218}
}
@misc{fds366270,
Author = {Drea, CM and Coscia, EM and Glickman, SE},
Title = {Hyenas},
Pages = {637-645},
Booktitle = {Encyclopedia of Reproduction},
Year = {2018},
Month = {January},
ISBN = {9780128151457},
url = {http://dx.doi.org/10.1016/B978-0-12-809633-8.20611-0},
Abstract = {The four, extant species of hyenids (aardwolves, striped
hyenas, brown hyenas, and spotted hyenas) are compared and
contrasted. Despite belonging to a small family of
carnivorans, these species show a wide range of social
systems (from solitary to gregarious), mating systems (from
monogamy to promiscuity), and feeding ecologies (from
myrmecophagy, through solitary scrounging, to group
hunting). The most remarkable differences, however, concern
their reproductive biology: Whereas the first three species
show the typical mammalian pattern of sexual dimorphism, the
fourth - the spotted hyena - shows the most extreme form of
sexual monomorphism evidenced by any mammal. The female
spotted hyena is behaviorally and morphologically
“masculinized,” being larger than the male, socially
dominant over the male, and possessing external reproductive
anatomy that bears striking resemblance to that of the male.
Notably, the female has no “external” vagina; instead,
the urogenital canal passes through a peniform clitoris,
providing the female spotted hyena with a singular opening
through which she urinates, copulates, and gives birth.
Decades of experimental, endocrine, morphological, and
histological studies have been aimed at demystifying this
evolutionary puzzle. The developmental trajectory of female,
and male, reproductive structures suggest that a combination
of genetic and endocrine factors, including androgen
production by the fetal ovary and placental metabolism of
androstenedione, operate in tandem during sexual
differentiation of the spotted hyena. But, formation of the
“masculine” genitalia of female Crocuta appears to
result from a unique mechanism that is unknown at this
time.},
Doi = {10.1016/B978-0-12-809633-8.20611-0},
Key = {fds366270}
}
@misc{fds44284,
Author = {Drea, C.M.},
Title = {Mammalian olfactory communication},
Volume = {1},
Pages = {369-374},
Booktitle = {Encyclopedia of Animal Behavior},
Publisher = {Westport, CT: Greenwood Press},
Editor = {M. Bekoff},
Year = {2004},
Key = {fds44284}
}
@misc{fds44286,
Author = {Drea, C.M.},
Title = {Spotted hyena development},
Volume = {2},
Pages = {495-500},
Booktitle = {Encyclopedia of Animal Behavior},
Publisher = {Westport, CT: Greenwood Press},
Editor = {M. Bekoff},
Year = {2004},
Key = {fds44286}
}
@misc{fds44287,
Author = {Drea, C.M.},
Title = {Social learning and intelligence in primates},
Volume = {2},
Pages = {715-717},
Booktitle = {Encyclopedia of Animal Behavior},
Publisher = {Westport, CT: Greenwood Press},
Editor = {M. Bekoff},
Year = {2004},
Key = {fds44287}
}
@misc{fds44293,
Author = {Drea, C.M.},
Title = {There, there},
Pages = {55-57},
Booktitle = {The Smile of a Dolphin: Remarkable Accounts of Animal
Emotions},
Publisher = {Random House/Discovery Books},
Editor = {M. Bekoff},
Year = {2000},
Key = {fds44293}
}
@misc{fds44295,
Author = {Drea, C.M. and Coscia, E.M. and Glickman, S.E.},
Title = {Hyenas},
Volume = {2},
Series = {Encyclopedia of Reproduction},
Pages = {718-725},
Publisher = {San Diego: Academic Press},
Editor = {E. Knobil and J. Neill and P. Licht},
Year = {1999},
Key = {fds44295}
}
%% Other
@misc{fds222016,
Author = {Grogan, K. and Drea, C.M.},
Title = {Using next-generation sequencing to investigate genetic
health in a threatened primate},
Journal = {Paper presented at the 26th International Congress of
Conservation Biology, Baltimore, MD},
Year = {2013},
Key = {fds222016}
}
@misc{fds222014,
Author = {Kulahci, I.G. and Drea, C.M. and Rubenstein, D.I. and Ghazanfar,
A.A.},
Title = {Ring-tailed lemurs (Lemur catta) recognize familiar
individuals by matching odors and vocalizations},
Journal = {Poster presented at the 49th Annual Meeting of the Animal
Behavior Society, Albuquerque, NM},
Year = {2012},
Key = {fds222014}
}
@misc{fds222015,
Author = {Crawford, J.C. and Drea, C.M.},
Title = {Plasticity in primate olfactory signals: Testing the
hormonal modulation of scent via natural and controlled
experiments},
Journal = {Paper presented at the 28th Annual Meeting of the
International Society of Chemical Ecology, Vilnius,
Lithuania},
Year = {2012},
Key = {fds222015}
}
@misc{fds222011,
Author = {Petty, J.M. and Drea, C.M.},
Title = {Behavioral neuroendocrinology in female-dominant versus
co-dominant Eulemur},
Journal = {Paper to be presented at the Joint Meeting of the Animal
Behavior Society and the International Ethological
Conference, Bloomington, IN},
Year = {2011},
Key = {fds222011}
}
@misc{fds222012,
Author = {Greene, L. and Dubay, G.R. and Drea, C.M.},
Title = {Sending mixed signals: olfactory communication in
Coquerel’s sifakas, Propithecus coquereli},
Journal = {Poster presented at the Joint Meeting of the Animal Behavior
Society and the International Ethological Conference,
Bloomington, IN},
Year = {2011},
Key = {fds222012}
}
@misc{fds222013,
Author = {Rushmore, J and Leonhardt, S.D. and Drea, C.M.},
Title = {Sight or scent: Sensory reliance in detecting food quality
by foraging lemurs reflects differing feeding
ecologies},
Journal = {Paper presented at the 96th Annual Meeting of the Ecological
Society of America, Austin, TX},
Year = {2011},
Key = {fds222013}
}
@misc{fds222004,
Author = {Sacha, C.R. and Dubay, G.R. and Drea, C.M.},
Title = {Comparative study of olfactory communication in
Eulemurs.},
Journal = {Poster presented at the 239th National Meeting of the
American Chemical Society. San Francisco,
CA},
Year = {2010},
Key = {fds222004}
}
@misc{fds222005,
Author = {Kesler, W.W. III and Sacha, C.R. and Drea, C.M. and Dubay, G.
R.},
Title = {Seasonal variation of characteristic scent compounds in
Eulemurs using gc/ms analysis.},
Journal = {Poster presented at the 239th National Meeting of the
American Chemical Society. San Francisco,
CA},
Year = {2010},
Key = {fds222005}
}
@misc{fds222007,
Author = {delBarco-Trillo†, J. and Burkert, B.A. and Goodwin, T.E. and Drea, C.M.},
Title = {Phylogenetic and socioecological patterns in the urinary
cues of prosimians.},
Journal = {Paper presente at the 47th Annual Meeting of the Animal
Behavior Society, Williamsburg, Virginia},
Year = {2010},
Key = {fds222007}
}
@misc{fds222008,
Author = {Drea, C.M. and Boulet, M. and Charpentier, M.J.E. and Crawford,
J.C.},
Title = {Message ‘scent’: lemurs detect honest olfactory
ornaments in females},
Journal = {Paper presented at the 47th Annual Meeting of the Animal
Behavior Society, Williamsburg, Virginia},
Year = {2010},
Key = {fds222008}
}
@misc{fds222009,
Author = {Crawford, J.C. and Boulet, M. and Drea, C.M.},
Title = {Smelling wrong: hormonal contraception alters critical
female odor cues},
Journal = {Paper presented by Drea at the 47th Annual Meeting of the
Animal Behavior Society, Williamsburg, Virginia},
Year = {2010},
Key = {fds222009}
}
@misc{fds168401,
Author = {Boulet, M. and Crawford, J.C. and Drea, C.M.},
Title = {Quand l’odeur n’est plus sexy: la contraception
hormonale altère les signaux olfactifs des femelles
lémurs},
Journal = {Paper presented at the Meeting of the Société Québécoise
pour l’étude biologique du comportement, Trois-Rivières,
Québec},
Year = {2009},
Key = {fds168401}
}
@misc{fds164610,
Author = {Charpentier, M. and Boulet, M. and Crawford, J. and Drea,
C.M.},
Title = {Olfaction as a mechanism guiding kin recognition and mate
choice in a primate species},
Journal = {Paper presented at the Meeting of the International Society
of Chemical Ecology. Neuchâtel, Switzerland},
Year = {2009},
Key = {fds164610}
}
@misc{fds164611,
Author = {Boulet, M. and Charpentier, M. and Crawford, J. and Drea,
C.M.},
Title = {Scent gland secretions signal genetic relatedness in a
promiscuous social primate},
Journal = {Paper presented at the 3rd Meeting of the Canadian Society
for Ecology and Evolution. Nova Scotia, Canada},
Year = {2009},
Key = {fds164611}
}
@misc{fds164612,
Author = {Crawford, J. and Charpentier, M. and Boulet, M. and Drea,
C.M.},
Title = {Lemurs discriminate conspecific scent based on individual
heterozygosity and pairwise relatedness},
Journal = {Paper presented at the Annual Meeting of the Society for
Integrative and Comparative Biology, Boston,
Mass},
Year = {2009},
Key = {fds164612}
}
@misc{fds164613,
Author = {Sacha, C. and Dubay, G. and Boulet, M. and Drea,
C.M.},
Title = {Olfactory signals in eight species of Eulemur vary by
species, sex, and gland},
Journal = {Poster presented at the National Meeting of the American
Chemical Society. Salt Lake City, UT},
Year = {2009},
Key = {fds164613}
}
@misc{fds154074,
Author = {Sacha, C. and Dubay, G. and Boulet, M. and Drea,
C.M.},
Title = {A comparative study of olfactory signals in two species of
Eulemur},
Journal = {Poster presented at the National Meeting of the American
Chemical Society. New Orleans, LA},
Year = {2008},
Key = {fds154074}
}
@misc{fds154075,
Author = {Boulet, M. and Charpentier, M. and Drea, C.M.},
Title = {The sweet smell of success: Scent marks advertise the
genetic quality of female lemurs.},
Journal = {Paper presented at the 2nd Meeting of the Canadian Society
for Ecology and Evolution. Vancouver, BC,
Canada},
Year = {2008},
Key = {fds154075}
}
@misc{fds154076,
Author = {Boulet, M. and Charpentier, M. and Drea, C.M.},
Title = {The sweet smell of success: Scent marks advertise the
genetic quality of lemurs.},
Journal = {Podium presentation by Drea, 22nd Congress of the
International Primatological Society. Edinburgh,
UK},
Year = {2008},
Key = {fds154076}
}
@misc{fds154077,
Author = {Drea, C.M.},
Title = {Sexual differentiation in unconventional
mammals.},
Journal = {Invited Speakers Program, 88th Annual Convention of the
Western Psychological Association. Irvine,
CA},
Year = {2008},
Key = {fds154077}
}
@misc{fds154078,
Author = {Drea, C.M.},
Title = {Cooperation in carnivores: Implications for primate
cooperation studies. Symposium on Cooperation, Reciprocity
and Responses to Inequity.},
Journal = {22nd Congress of the International Primatological Society.
Edinburgh, UK},
Year = {2008},
Key = {fds154078}
}
@misc{fds140930,
Author = {Brannon, E. and Drea, C. and O’Neill, M. and Platt, M. and Williams, C. and Zehr S.},
Title = {Lemur catta, head to toe: A montage of research at the Duke
Lemur Center},
Journal = {Poster presented at the International Congress on
Prosimians. Ithala, South Africa},
Year = {2007},
Month = {July},
Key = {fds140930}
}
@misc{fds140928,
Author = {Charpentier, M. and Drea, C.M.},
Title = {Inbreeding and health in a captive lemur
population},
Journal = {Paper presented at the 30th Meeting of the American Society
of Primatologists. Winston-Salem, NC},
Year = {2007},
Month = {June},
Key = {fds140928}
}
@misc{fds140929,
Author = {Boulet, M. and Charpentier, M. and Drea, C.M.},
Title = {Smelling right: do olfactory cues signal genetic
constitution in male ringtailed lemurs (Lemur
catta)?},
Journal = {Paper presented at the 1st Meeting of the Canadian Society
for Ecology and Evolution. Toronto, Ontario,
Canada},
Year = {2007},
Month = {May},
Key = {fds140929}
}
@misc{fds140927,
Author = {Chen, C.J. and Jackson, S.R. and Weddell, M.E. and Goodwin, T.E. and Drea, C.M. and Schulte, B.A.},
Title = {Use of automated SPDE/GC-MS, novel macros, and pattern
recognition techniques in a search for African elephant
urinary pheromones},
Journal = {Poster presented at the National Meeting of the American
Chemical Society, Chicago, Illinois},
Year = {2007},
Month = {March},
Key = {fds140927}
}
@misc{fds51255,
Author = {Drea, C.M.},
Title = {Are female ringtailed lemurs (Lemur catta) naturally
‘masculinized’?: Insights from the spotted hyena
(Crocuta crocuta) model},
Journal = {Podium presentation, 43rd Annual Meeting of the Animal
Behavior Society, Snowbird, Utah},
Year = {2006},
Month = {August},
Key = {fds51255}
}
@misc{fds51256,
Author = {Drea, C.M. and Scordato, E.S.},
Title = {Chemical composition of scent marks in Lemur catta:
individual scent signatures and seasonal
variation},
Journal = {Invited podium presentation, 11th Conference on ‘Chemical
Signals in Vertebrates’ Chester, UK},
Year = {2006},
Month = {July},
Key = {fds51256}
}
@misc{fds51254,
Author = {Drea, C.M.},
Title = {Costs of female ‘androgenization:’ effects of prenatal
anti-androgen treatment on adult reproductive
success},
Journal = {Invited podium presentation, Conference of Collaborators on
the UCB Hyena Project, University of California, Berkeley,
CA},
Year = {2006},
Month = {February},
Key = {fds51254}
}
@misc{fds44343,
Author = {Drea, C.M.},
Title = {Could female ringtailed lemurs be ‘masculinized’ by
maternal androgens?},
Journal = {Podium presentation, Annual Meeting of the Society for
Integrative and Comparative Biology, Orlando,
Florida},
Year = {2006},
Month = {January},
Key = {fds44343}
}
@misc{fds44344,
Author = {Roth, J.D. and Wiesel, I and Drea, C.M.},
Title = {Variation in seal consumption by brown hyenas in the Namib
desert estimated using stable isotopes},
Journal = {Paper presented at the Annual Meeting of the Society for
Integrative and Comparative Biology, Orlando,
Florida},
Year = {2006},
Month = {January},
Key = {fds44344}
}
@misc{fds44345,
Author = {Scordato, E. and Drea, C.M.},
Title = {Sex-specific variation in ringtailed lemur (Lemur catta)
olfactory communication},
Journal = {Paper presented at the Annual Meeting of the Society for
Integrative and Comparative Biology, Orlando,
Florida},
Year = {2006},
Month = {January},
Key = {fds44345}
}
@misc{fds44346,
Author = {Scordato, E. and Drea, C.M.},
Title = {Odor discrimination in ringtailed lemurs (Lemur catta):
variation in chemical composition and behavioral
response},
Journal = {Paper presented at the 42nd Annual Meeting of the Animal
Behavior Society, Snowbird, Utah},
Year = {2005},
Month = {August},
Key = {fds44346}
}
@misc{fds44347,
Author = {Place, N.J. and Coscia, E.M. and Dahl, N.J. and Drea, C.M. and Holekamp, K.E. and Sisk, C.L. and Weldele, M.L. and Glickman,
S.E.},
Title = {Paradoxical effects of maximal androgen blockade on sex
hormone concentrations in pregnant spotted
hyenas},
Journal = {Paper presented at the 38th Annual Meeting of the Society
for the Study of Reproduction, Québec City, Québec,
Canada},
Year = {2005},
Month = {July},
Key = {fds44347}
}
@misc{fds30072,
Author = {Drea, C.M. and Scordato, E. and Fitzpatrick,
C.},
Title = {Social behavior and olfactory communication in ringtailed
lemurs (Lemur catta): form and function},
Series = {Podium presentation, 41st Annual Meeting of the Animal
Behavior Society, Oaxaca, Mexico},
Year = {2004},
Month = {July},
Key = {fds30072}
}
@misc{fds30097,
Author = {Drea, C.M.},
Title = {Bateman revisited: Sexually assertive female primates and
their cryptic reproductive tactics},
Series = {Invited podium presentation, Symposium on Bateman’s
Principle: Is it time for a re-evaluation? Annual Meeting of
the Society for Integrative and Comparative Biology, New
Orleans, LA},
Year = {2004},
Month = {January},
Key = {fds30097}
}
@misc{fds30073,
Author = {Place N.J. and Weldele, M.L. and Coscia, E.M. and Glickman, S.E. and Drea, C.M. and Lue, T. F. and Baskin, L. S.},
Title = {Mating with the highly masculinized female spotted hyena:
size and shape matter},
Series = {Paper presented at the Western Regional Conference on
Comparative Endocrinology, Boulder, CO},
Year = {2003},
Month = {March},
Key = {fds30073}
}
@misc{fds30098,
Author = {Drea, C.M.},
Title = {Evolution and social behavior: reproductive strategies in
female primates},
Series = {Invited podium presentation, Symposium on Evolution and
Psychology (in Honor of Stephen J. Gould). 2nd Annual
Sandhills Regional Psychology Conference, Fayetteville State
University, Fayetteville, NC},
Year = {2003},
Month = {March},
Key = {fds30098}
}
@misc{fds30074,
Author = {Drea, C.M. and Place, N.J. and Weldele, M.L. and Coscia, E.M. and Licht, P. and Glickman, S.E.},
Title = {Reproduction in spotted hyenas: Fetal androgens are
prerequisite for male mating but incur direct costs in
females},
Series = {Paper presented at the 39th Annual Meeting of the Animal
Behavior Society, Bloomington, IN},
Year = {2002},
Month = {July},
Key = {fds30074}
}
@misc{fds30076,
Author = {Place, N.J. and Drea, C.M. and Holekamp, K.E. and Weldele, M.L. and Coscia, E.M. and Glickman, S.E.},
Title = {Sex differences and effects of prenatal anti-androgens on LH
secretion in spotted hyenas},
Series = {Paper presented at the Annual Meeting of the Society of
Integrative and Comparative Biology, Anaheim,
CA},
Year = {2002},
Month = {January},
Key = {fds30076}
}
@misc{fds30077,
Author = {Drea, C.M. and Vignieri, S.N. and Cunningham, S.B. and Glickman,
S.E.},
Title = {A rose by any other name... : response to olfactory cues in
spotted hyenas},
Series = {Paper presented at the 38th Annual Meeting of the Animal
Behavior Society, Corvallis, OR},
Year = {2001},
Month = {July},
Key = {fds30077}
}
@misc{fds30100,
Author = {Drea, C.M.},
Title = {Female urogenital ‘masculinization’ in
prosimians},
Series = {Invited paper presented at the Conference of Collaborators
on the UC Hyena Project, University of California, Berkeley,
CA},
Year = {2001},
Month = {January},
Key = {fds30100}
}
@misc{fds30101,
Author = {Drea, C.M.},
Title = {Effects of anti-androgens administered during gestation on
development of offspring: Morphology and gonadal
steroids},
Series = {Invited paper presented at the Conference of Collaborators
on the UC Hyena Project, University of California, Berkeley,
CA},
Year = {2001},
Month = {January},
Key = {fds30101}
}
@misc{fds30102,
Author = {Drea, C.M.},
Title = {Sensory systems and communication: Reaction to olfactory
stimuli},
Series = {Invited paper presented at the Conference of Collaborators
on the UC Hyena Project, University of California, Berkeley,
CA},
Year = {2001},
Month = {January},
Key = {fds30102}
}
@misc{fds30103,
Author = {Drea, C.M.},
Title = {Hormones and social behavior: Play and aggression},
Series = {Invited paper presented at the Conference of Collaborators
on the UC Hyena Project, University of California, Berkeley,
CA},
Year = {2001},
Month = {January},
Key = {fds30103}
}
@misc{fds30104,
Author = {Drea, C.M.},
Title = {Social cognition and cooperation in the spotted
hyena},
Series = {Conference on Animal Social Complexity and Intelligence. The
Chicago Academy of Sciences, Chicago, IL},
Year = {2000},
Month = {August},
Key = {fds30104}
}
@misc{fds30105,
Author = {Drea, C.M.},
Title = {Do chimpanzees know what others know?},
Series = {Symposium on the Human Adaptation for Culture. Center for
Interdisciplinary Studies in Science and Cultural Theory,
Duke University, Durham, NC},
Year = {2000},
Month = {February},
Key = {fds30105}
}
@misc{fds30106,
Author = {Drea, C.M.},
Title = {Modeling cooperative hunting in a social
carnivore},
Series = {Symposium on Natural Cognition: Cooperation. Max Plank
Institute for Evolutionary Anthropology, Leipzig,
Germany},
Year = {1999},
Month = {June},
Key = {fds30106}
}
@misc{fds30078,
Author = {Drea, C.M. and Weldele, M. and Forger, N.G. and Cosica, E.M. and Frank, L.G. and Licht, P. and Glickman, S.E.},
Title = {Masculinization in the spotted hyena (Crocuta crocuta):
Effects of prenatal anti-androgens on infant genital
development and hormone production},
Series = {Poster presented at the 2nd Annual Meeting of the Society
for Behavioral Neuroendocrinology, Atlanta,
GA},
Year = {1998},
Month = {June},
Key = {fds30078}
}
@misc{fds30107,
Author = {Drea, C.M.},
Title = {The Berkeley Hyena Project},
Series = {District VIII Meeting of the American Association for
Laboratory Animal Science, Berkeley, CA},
Year = {1998},
Month = {May},
Key = {fds30107}
}
@misc{fds30108,
Author = {C. Drea},
Title = {Dispelling myths about spotted hyenas},
Series = {Family Wildlife Festival on Leaders of the Pack: Wild Dogs
Among Us, Lindsay Wildlife Museum, Walnut Creek,
CA},
Year = {1998},
Month = {February},
Key = {fds30108}
}
@misc{fds30109,
Author = {Drea, C.M.},
Title = {Social interactions and the primate amygdala},
Series = {Workshop on Evaluating the Behavioral Effects of Amygdala
Damage. University of California at San Diego, Department of
Psychiatry, San Diego, CA},
Year = {1997},
Month = {March},
Key = {fds30109}
}
@misc{fds30079,
Author = {Drea, C.M. and Neves, A. and Lopez, V. and Glickman,
S.E.},
Title = {Cooperation in captive spotted hyenas (Crocuta
crocuta)},
Series = {Paper presented at the 33rd Annual Meeting of the Animal
Behavior Society, Flagstaff, AZ},
Year = {1996},
Month = {August},
Key = {fds30079}
}
@misc{fds30080,
Author = {Drea, C.M. and Weldele, M. and Frank, L.G. and Licht, P. and Glickman,
S.E.},
Title = {Effects of prenatal anti-androgen treatment on genital
development in spotted hyenas (Crocuta crocuta)},
Series = {Paper presented at the Western Regional Conference on
Comparative Endocrinology, Berkeley, CA},
Year = {1996},
Month = {March},
Key = {fds30080}
}
@misc{fds30081,
Author = {Drea, C.M. and Hawk, J.E. and Glickman, S.E.},
Title = {The emergence of affiliative behavior in infant spotted
hyenas (Crocuta crocuta)},
Series = {Poster presented at the New York Academy of Sciences
Conference on the Integrative Neurobiology of Affiliation,
Washington, DC},
Year = {1996},
Month = {March},
Key = {fds30081}
}
@misc{fds30082,
Author = {Glickman, S.E. and Drea, C.M. and Weldele, M. and Frank, L.G. and Cunha, G. and Licht, P.},
Title = {Sexual differentiation of the female spotted hyena (Crocuta
crocuta)},
Series = {Paper presented at the XXIVth International Ethological
Conference, Honolulu, HI},
Year = {1995},
Month = {August},
Key = {fds30082}
}
@misc{fds30083,
Author = {Drea, C.M. and Wallen, K.},
Title = {Social modulation of performance on learning tasks in rhesus
monkeys},
Series = {Paper presented at the XXVth Annual Symposium of the Jean
Piaget Society: Piaget, Evolution, and Development,
Berkeley, CA},
Year = {1995},
Month = {June},
Key = {fds30083}
}
@misc{fds30084,
Author = {Glickman, S.E. and Drea, C.M. and Weldele, M. and Frank, L.G. and Cunha, G. and Licht, P.},
Title = {Sexual differentiation of the female spotted hyena (Crocuta
crocuta)},
Series = {Paper presented at the Keystone Symposium on the Molecular
Basis for Differences Between the Sexes, Tamarron,
CO},
Year = {1995},
Month = {February},
Key = {fds30084}
}
@misc{fds30085,
Author = {Drea, C.M. and Hawk, J.E. and Glickman, S.E.},
Title = {Aggression decreases as play emerges in infant spotted
hyenas (Crocuta crocuta)},
Series = {Paper presented at the 31st Annual Meeting of the Animal
Behavior Society, Seattle, WA},
Year = {1994},
Month = {July},
Key = {fds30085}
}
@misc{fds30087,
Author = {Drea, C.M. and Mann, D.R. and Akinbami, M.A. and Wallen,
K.},
Title = {Neonatal testosterone and handedness in rhesus monkeys
(Macaca mulatta)},
Series = {). Paper presented at the 30th Annual Meeting of the Animal
Behavior Society, Davis, CA},
Year = {1993},
Month = {July},
Key = {fds30087}
}
@misc{fds30088,
Author = {Drea, C.M. and Wallen, K.},
Title = {Social cognition in subordinate rhesus monkeys (Macaca
mulatta): Failure to learn or failure to
perform?},
Series = {Paper presented at the XIVth Congress of the International
Primatological Society, Strasbourg, France},
Year = {1992},
Month = {August},
Key = {fds30088}
}
@misc{fds30089,
Author = {Drea, C.M.},
Title = {Social status and performance on learning tasks in rhesus
monkeys},
Series = {. Paper presented at the 29th Annual Meeting of the Animal
Behavior Society, Kingston, Ontario},
Year = {1992},
Month = {June},
Key = {fds30089}
}
@misc{fds30090,
Author = {Drea, C.M. and Wallen, K.},
Title = {Color discrimination and learning set formation in a social
group of rhesus monkeys (Macaca mulatta)},
Series = {Poster presented at the 26th Annual Meeting of the Animal
Behavior Society, Binghamton, NY,},
Year = {1990},
Month = {July},
Key = {fds30090}
}
@misc{fds30091,
Author = {Drea, C. and Wallen, K.},
Title = {Color discrimination and color reversal acquisition in
group-living rhesus monkeys (Macaca mulatta)},
Series = {Paper presented at the XIIIth Annual Meeting of the American
Society of Primatologists. Davis, CA},
Year = {1990},
Month = {July},
Key = {fds30091}
}
@misc{fds30092,
Author = {Hohman, T.C. and Nagata, M and Nishimura, C. and Drea, C. and Kinoshita, J.H. and Robison, W.G., Jr.},
Title = {Aldose reductase inhibitors and the depletion of
myo-inositol in cultured lens cells},
Series = {Paper presented at the Annual Meeting of the Association for
Research in Vision and Ophthalmology, Fort Lauderdale,
FL},
Year = {1987},
Month = {March},
Key = {fds30092}
}
@misc{fds30093,
Author = {Drea, C.M. and Katz, M.L. and Robison, W.G., Jr. and Hess,
H.H.},
Title = {Influence of early photoreceptor cell degeneration on
lipofuscin in the retinal pigment epithelium},
Series = {Poster presented at the 16th Annual meeting of the American
Aging Association},
Year = {1987},
Key = {fds30093}
}
@misc{fds30094,
Author = {Drea, C.M. and Robison, W.G., Jr.},
Title = {Rod outer segment degeneration and lipid granule formation
in the rat retina},
Series = {Paper presented at the Summer Symposia Series of the
National Eye Institute, National Institutes of Health,
Bethesda, MD},
Year = {1985},
Month = {August},
Key = {fds30094}
}
@misc{fds30096,
Author = {Robison, W.G., Jr. and Hohman, T. and Katz, M. and Drea,
C.},
Title = {Retinal capillaries: characterization of the thickened
basement membranes in diabetic, galactosemic, and senescent
rats},
Series = {Paper presented at the Annual Meeting of the Association for
Research in Vision and Ophthalmology, Fort Lauderdale,
FL},
Year = {1985},
Month = {March},
Key = {fds30096}
}