Evidence for a bacterial mechanism for group-specific social odors among hyenas

Theis, Kevin R.; Schmidt, Thomas M.; Holekamp, Kay E.

doi:10.1038/srep00615

Cited by 118 publications

(107 citation statements)

References 55 publications

(108 reference statements)

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“…We also did not find a consistent effect of sex on the bacterial or VFA profiles of spotted hyena paste at the population level. The bacterial and odor profiles of spotted hyena pastes are generally clan specific (15,16). The purported mechanism for clan-specific paste odors is that clan members develop more homogeneous paste bacterial communities than the general population through cross-infection fostered by consistently overmarking the same pasting sites (12,15,16,40).…”

Section: Discussionmentioning

confidence: 99%

“…The bacterial and odor profiles of spotted hyena pastes are generally clan specific (15,16). The purported mechanism for clan-specific paste odors is that clan members develop more homogeneous paste bacterial communities than the general population through cross-infection fostered by consistently overmarking the same pasting sites (12,15,16,40). Indeed, in this study, the structures of bacterial communities in the pastes of spotted hyena males and lactating females were more variable in the general MMNR population than in the Talek clan [PERMDISP; MMNR (0.387 ± 0.092) vs. Talek (0.292 ± 0.059), P = 0.0017].…”

Section: Discussionmentioning

confidence: 99%

“…They represented the general MMNR population (nine males/10 females from >10 clans) as well as a single, intensively studied clan (seven males/seven lactating females/seven pregnant females from the Talek clan). Only one individual, CNLF428, appeared in our prior study (15). Females from the general MMNR population were lactating when sampled.…”

Section: Discussionmentioning

confidence: 99%

“…As a consequence, evaluations of the hypothesis typically have concluded that the bacterial diversity in integumental scent gland secretions is insufficient to underlie the observed diversity of chemical signals (6,14). In a recent study, we used next-generation sequencing to thoroughly survey the bacterial communities in the scent gland secretions of adult female spotted hyenas, Crocuta crocuta (15). That study revealed more types of bacteria than the 15 previous surveys of specialized mammalian scent glands combined and demonstrated that most of these bacteria were members of fermentative, odor-producing clades.…”

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confidence: 99%

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Symbiotic bacteria appear to mediate hyena social odors

Theis

Venkataraman²,

Dycus³

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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189

169

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All animals harbor beneficial microbes. One way these microbes can benefit their animal hosts is by increasing the diversity and efficacy of communication signals available to the hosts. The fermentation hypothesis for mammalian chemical communication posits that bacteria in the scent glands of mammals generate odorous metabolites used by their hosts for communication and that variation in host chemical signals is a product of underlying variation in the bacterial communities inhabiting the scent glands. An effective test of this hypothesis would require accurate surveys of the bacterial communities in mammals' scent glands and complementary data on the odorant profiles of scent secretions-both of which have been historically lacking. Here we use next-generation sequencing to survey deeply the bacterial communities in the scent glands of wild spotted and striped hyenas. We show that these communities are dominated by fermentative bacteria and that the structures of these communities covary with the volatile fatty acid profiles of scent secretions in both hyena species. The bacterial and volatile fatty acid profiles of secretions differ between spotted and striped hyenas, and both profiles vary with sex and reproductive state among spotted hyenas within a single social group. Our results strongly support the fermentation hypothesis for chemical communication, suggesting that symbiotic bacteria underlie species-specific odors in both spotted and striped hyenas and further underlie sex and reproductive state-specific odors among spotted hyenas. We anticipate that the fermentation hypothesis for chemical communication will prove broadly applicable among scent-marking mammals as others use the technical and analytical approaches used here.animal behavior | animal communication | microbiome

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

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Symbiotic bacteria appear to mediate hyena social odors

Theis

Venkataraman²,

Dycus³

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

189

169

View full text Add to dashboard Cite

show abstract

“…More recent cultivationindependent studies of spotted hyaenas (Crocuta crocuta) and striped hyaenas (Hyaena hyaena) showed that the bacterial and SCFA profiles of the two hyaena species differ and that the two profiles covary within each hyaena species. Further, among spotted hyaenas, the two profiles are social group-specific, and reflect sex and reproductive state among members of the same social group [49][50][51]. Similar patterns are evident among mammals that communicate via urine marking as well.…”

Section: Chemosensory Detection Of Microbial Productsmentioning

confidence: 82%

Animal–microbe interactions and the evolution of nervous systems

Eisthen

Theis

2016

Phil. Trans. R. Soc. B

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One contribution of 16 to a discussion meeting issue 'Homology and convergence in nervous system evolution'. Animals ubiquitously interact with environmental and symbiotic microbes, and the effects of these interactions on animal physiology are currently the subject of intense interest. Nevertheless, the influence of microbes on nervous system evolution has been largely ignored. We illustrate here how taking microbes into account might enrich our ideas about the evolution of nervous systems. For example, microbes are involved in animals' communicative, defensive, predatory and dispersal behaviours, and have likely influenced the evolution of chemoand photosensory systems. In addition, we speculate that the need to regulate interactions with microbes at the epithelial surface may have contributed to the evolutionary internalization of the nervous system.

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The “Secret” in Secretions: Methodological Considerations in Deciphering Primate Olfactory Communication

Drea

Boulet

delBarco‐Trillo

et al. 2013

American J Primatol

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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.

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Evidence for a bacterial mechanism for group-specific social odors among hyenas

Cited by 118 publications

References 55 publications

Symbiotic bacteria appear to mediate hyena social odors

Symbiotic bacteria appear to mediate hyena social odors

Animal–microbe interactions and the evolution of nervous systems

The “Secret” in Secretions: Methodological Considerations in Deciphering Primate Olfactory Communication

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