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    Christine Drea

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    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... more
    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 o...
    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,... more
    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 structure, across scales, to improve understanding of host-microbe symbiosis during dysbiosis and recovery. We experimentally administered a broad-spectrum antibiotic alone or with subsequent fecal transfaunation to healthy, male ring-tailed lemurs (Lemur catta) and longitudinally tracked the diversity, composition, associations, and resistomes of their gut microbiota. Whereas microbial diversity recovered rapidly in lemurs, antibiotics caused long-term instability in community composition – effects that were attenuated by fecal transfaunation. Antibiotic resistance genes, which were universally present, including in treatment-naïve subjects, incr...
    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... more
    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 (<i>Eulemur</i> spp.) and the folivorous sifakas (<i>Propithecus</i> 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.
    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... more
    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.
    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,... more
    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 withinEulemur, 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 12Eulemurbrains 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...
    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.... more
    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...
    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... more
    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 re...
    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... more
    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 we...
    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... more
    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 p...
    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... more
    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 acces...
    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... more
    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, folivorous primate endemic to Madagascar - is precariously susceptible to cryptosporidiosis under captive conditions. If left untreated, infection can rapidly advance to morbidity and death. Objective: 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. Design: Using 16S sequencing of DNA extracted from sifaka fecal samples, we compared the microbial communities of healthy sifakas to those of infected individuals, acr...
    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... more
    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 base...
    Supplementary materials [119]. (DOCX 43Â kb)
    BackgroundInter-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... more
    BackgroundInter-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...
    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... more
    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...
    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... more
    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.
    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... more
    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 i...
    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... more
    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 ...
    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... more
    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 behaviour within and across generations. In 22 wild meerkat (Suricata suricatta) clans, we show that matriarchs 1) express peak androgen concentrations during late gestation, 2) when displaying peak feeding competition, dominance, and evictions, and 3) relative to subordinates, produce offspring that are more aggressive in early development. Late-gestation, antiandrogen treatment of matriarchs 4) reduced their dominance behaviour, was associated with infrequent evictions, decreased social centrality within the clan, 5) increased aggression in cohabiting subordinate dams, and 6) reduced their offspring’s aggression. These effects implicate androg...
    ABSTRACTDiversity 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... more
    ABSTRACTDiversity 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 identification or mate choice. To investigate MHC-based signaling and recipient sensitivity, we test for odor-gene covariance and behavioral discrimination of MHC diversity and pairwise dissimilarity, under the good genes and good fit paradigms, in a strepsirrhine primate, the ring-tailed lemur (Lemur catta). First, we coupled genotyping with gas chromatography-mass spectrometry to investigate if diversity of the MHC-DRB gene is signaled by the chemical diversity of lemur genital scent gland secretions. We also assessed if the chemical similarity between individuals correlated with their MHC similarity. Next, we assessed if lemurs di...
    This is the peer-reviewed, manuscript version of the following article: DelBarco-Trillo, J and Greene, L K and Goncalves, I B and Fenkes, M and Wisse, J H and Drewe, J A and Manser, M B and Clutton-Brock, T and Drea, C M (2016) Beyond... more
    This is the peer-reviewed, manuscript version of the following article: DelBarco-Trillo, J and Greene, L K and Goncalves, I B and Fenkes, M and Wisse, J H and Drewe, J A and Manser, M B and Clutton-Brock, T and Drea, C M (2016) Beyond aggression: Androgen-receptor blockade modulates social interaction in wild meerkats. Hormones and Behaviour, 78 (1). pp. 95-106. The final version is available online via http://dx.doi.org/10.1016/j.yhbeh.2015.11.001. © 2016. This manuscript version is made available under the CC-BY-NC-ND 4.0 license http://creativecommons.org/licenses/by-nc-nd/4.0/. The full details of the published version of the article are as follows:
    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... more
    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), serum estradiol (E), 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 abortio...
    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... more
    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 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 resisto...
    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,... more
    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 conce...
    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... more
    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 an...
    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... more
    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 bacteri...

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