Christine Drea

• B.S., M.A., Ph.D.
• Professor (Full) at Duke University

Aggression and its neurochemical modulators are typically studied in males, leaving the mechanisms of female competitive aggression or dominance largely unexplored. To better understand how competitive aggression is regulated in the primate brain, we used receptor autoradiography to compare the neural distributions of oxytocin and vasopressin recep...

In oviparous vertebrates, maternal androgens can alter offspring immune function, particularly early in development, but the potential for negative health effects of maternal androgens in mammals remains unclear. We investigated the relation between maternal androgens, particularly in late gestation, and offspring health in the meerkat (Suricata su...

Introduction Mammalian reproductive and somatic development is regulated by steroid hormones, growth hormone (GH), and insulin-like growth factor-1 (IGF-1). Based largely on information from humans, model organisms, and domesticated animals, testosterone (T) and the GH/IGF-1 system activate sexually differentiated development, promoting male-biased...

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...

Vertebrate odorants are essential to communication, but their complex chemical compositions are challenging to study. Here, we optimize a workflow for gas chromatography-mass spectrometry analysis of vertebrate odorants to generate a sensitive, broadly applicable method for detecting diverse compounds. We develop a standard mixture of 24 compounds...

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...

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...

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, sp...

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...

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 verte...

Intraspecific aggression, which links to dominance in socially integrated vertebrates, enables the struggle over limited resources to improve survival and reproduction. Studies of intrasexual competition—one of Darwin’s two mechanisms of sexual selection—typically focus on reproductive consequences of androgen-mediated, male aggression over access...

Background 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, in...

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 aggressi...

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 b...

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 (Eul...

Background 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...

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 acq...

Background 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, in...

Background 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 endange...

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...

Female intrasexual competition can be intense in cooperatively breeding species, with the dominant breeder or matriarch limiting reproduction in subordinates via aggression, eviction or infanticide. In males, these tendencies bidirectionally link to testosterone, but in females, there has been no systematic investigation of androgen-mediated behavi...

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 (Lemu...

Antibiotics alter the diversity, structure, and dynamics of host-associated microbial consortia, including via development of antibiotic resistance; however, patterns of recovery from dysbiosis and methods to mitigate negative effects, remain poorly understood. We applied an ecological framework via long-term, integrated study of community structur...

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 tra...

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 understandin...

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 percept...

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 di...

Background 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...

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...

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...

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...

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 comparat...

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 sifak...

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 (c...

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,...

Animal communication depends on the honesty with which signallers convey 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...

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 odor may signal its MHC and influence partner id...

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 infa...

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 diff...

Background: 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 Cryptosporidium, causes a variety of digestive disorders that can be devastating and even lethal. The Coquerel’s sifaka (Propithecus coquereli) – an endangered, f...

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 c...

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 so...

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 aggress...

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 nonhu-man primate...

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 increas...

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 male...

Background 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 t...

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, espec...

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 studie...

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 morp...

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. Altho...

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...

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...

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 in...

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 territoria...

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 form...

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 undersc...

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...

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 th...

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 org...

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 t...

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...

Investigatory behavior during multi-sensory trials. Duration of behavior by two strepsirrhine species when investigating comparable (A) red foods and (B) green foods during multi-sensory trials. Presented is the time spent (mean ± standard error of mean) looking at (shaded bars) and sniffing (open bars) the food items. Numbers at the bottom of the...

Volatile compounds in test food items. Methods for extracting and characterizing the volatile compounds in test food items, and for comparing the volatile compositions of red versus greed food items. (DOCX)

Performance by a male sifaka. A strepsirrhine primate is seen selecting a higher-quality red leaf over a lower-quality green leaf during a baseline trial in which both visual and olfactory cues about the food items were available. (WMV)

Representative chromatograms of the most highly volatile chemicals detected from the multi-sensory panel of the test apparatus, using an electronic sensor. Shown are the volatiles detected from (A) an empty, open drawer, (B) a green leaf inside a closed, but clear and solid ‘visual’ drawer, and (C) a green leaf inside a closed, but opaque and pierc...

Experimental study subjects and their food/sensory preferences. Bolded subjects represent those individuals that showed a relatively strong preference (P<0.05 or P<0.10 by G-test) for red food items during baseline trials. Only these bolded subjects were retained for analyses of performance during visual and olfactory trials, as these latter tests...

Comparison of G-test results for different categories of subjects during visual and olfactory trials. The subject categories included the following: (1) all of the subjects, (2) only those subjects that showed relatively strong preferences for red foods, and (3) only those subjects that showed significant preferences for red foods. Bolded G-tests a...

Subject visual status and its effect on performance. The effect of opsin gene polymorphism (i.e., dichromacy versus trichromacy) on the performance of strepsirrhine primates. (DOCX)

Analyses of the duration of investigatory behavior. Detailed analyses of looking and sniffing behavior of ruffed lemurs and ring-tailed lemurs. (DOCX)