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Research Article

Symbiotic bacteria appear to mediate hyena social odors

Kevin R. Theis, Arvind Venkataraman, Jacquelyn A. Dycus, Keith D. Koonter, Emily N. Schmitt-Matzen, Aaron P. Wagner, Kay E. Holekamp, and Thomas M. Schmidt
PNAS December 3, 2013 110 (49) 19832-19837; https://doi.org/10.1073/pnas.1306477110
Kevin R. Theis
Departments of aMicrobiology and Molecular Genetics and
bBEACON Center for the Study of Evolution in Action, Michigan State University, East Lansing, MI 48824
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  • For correspondence: theiskev@msu.edu
Arvind Venkataraman
Departments of aMicrobiology and Molecular Genetics and
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Jacquelyn A. Dycus
Departments of aMicrobiology and Molecular Genetics and
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Keith D. Koonter
Departments of aMicrobiology and Molecular Genetics and
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Emily N. Schmitt-Matzen
Departments of aMicrobiology and Molecular Genetics and
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Aaron P. Wagner
bBEACON Center for the Study of Evolution in Action, Michigan State University, East Lansing, MI 48824
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Kay E. Holekamp
bBEACON Center for the Study of Evolution in Action, Michigan State University, East Lansing, MI 48824
cZoology and
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Thomas M. Schmidt
Departments of aMicrobiology and Molecular Genetics and
bBEACON Center for the Study of Evolution in Action, Michigan State University, East Lansing, MI 48824
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  1. Edited by E. Peter Greenberg, University of Washington, Seattle, WA, and approved October 15, 2013 (received for review April 6, 2013)

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    Fig. 1.

    Differences in the bacterial (OTU) and VFA profiles of the pastes of adult spotted and striped hyenas. (A) A nonmetric multidimensional scaling (nMDS) plot showing a difference in structure (Bray–Curtis index) between the paste bacterial communities of adult spotted hyenas from the MMNR and adult striped hyenas from Laikipia and Shompole. (B) A Clearcut cladogram (26) of the prominent (i.e., top 15 based on average abundance) OTUs in the pastes of hyenas from the three populations and an accompanying heat map reflecting the mean abundances (out of 1,600 sequences) of these OTUs in pastes. These data were log-transformed before plotting (values in parentheses). Order- and genus-level classifications of OTUs, as determined by the Ribosomal Database Project’s Classifier (27), are noted also. (C) An nMDS plot showing a difference in structure between the paste VFA profiles of spotted and striped hyenas. (D) A heat map of the mean percent abundances of VFAs in the pastes of hyenas from the three populations. Sample sizes were 19, 13, and 9 for MMNR, Laikipia, and Shompole, respectively.

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    Fig. 2.

    Variation in the bacterial (OTU) and VFA profiles of the pastes of immigrant male, lactating female, and pregnant female spotted hyenas in the Talek clan. (A) An nMDS plot showing variation in the structure (Bray–Curtis index) of paste bacterial communities among Talek clan members. (B) A heat map of the mean abundances (out of 1,600 sequences) of the prominent (i.e., top 15 based on average abundance) OTUs in the pastes of Talek hyenas. These data were log-transformed before plotting (values in parentheses). (C) An nMDS plot showing variation in the structure of paste VFA profiles in Talek hyenas. (D) A heat map of the mean percent abundances of VFAs in the pastes of Talek hyenas. Seven hyenas were sampled from each reproductive class.

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    Fig. 3.

    Differences in the bacterial (OTU) and VFA profiles of the pastes of striped hyenas in Laikipia and Shompole. (A) An nMDS plot showing a difference between the structure (Bray–Curtis index) of paste bacterial communities in the Laikipia and Shompole populations. Lighter shading denotes samples obtained from juveniles. (B) A heat map of the mean abundances (out of 1,600 sequences) of the prominent (i.e., top 15 based on average abundance) OTUs in the pastes of striped hyenas. These data were log-transformed before plotting (values in parentheses). (C) An nMDS plot of the structures of paste VFA profiles in Laikipia and Shompole. (D) A heat map of the mean percent abundances of VFAs in the pastes of striped hyenas from the two populations. Twenty striped hyenas were sampled from Laikipia (8 male/12 female), and 13 (six male/ seven female) were sampled from Shompole.

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    Table 1.

    Nonparametric multivariate analyses of variance confirming that the bacterial (OTU) and VFA profiles of the pastes of Talek immigrant males, lactating females, and pregnant females vary

    Composition of paste OTU profiles (Jaccard index)
     Global effectF = 2.468, P = 0.0001
     Male vs.lactating femaleF = 2.485, P = 0.0011
     Male vs.pregnant femaleF = 3.070, P = 0.0020
     Lactating vs. pregnant femaleF = 1.757, P = 0.0177
    Structure of paste OTU profiles (Bray–Curtis index)
     Global effectF = 4.181, P = 0.0001
     Male vs.lactating femaleF = 3.789, P = 0.0006
     Male vs.pregnant femaleF = 6.023, P = 0.0007
     Lactating vs. pregnant femaleF = 2.411, P = 0.0398
    Structure of paste VFA profiles (Bray–Curtis index)
     Global effectF = 16.23, P = 0.0001
     Male vs.lactating femaleF = 5.779, P = 0.0116
     Male vs.pregnant femaleF = 43.81, P = 0.0008
     Lactating vs. pregnant femaleF = 9.209, P = 0.0069
    • Seven hyenas were sampled from each reproductive class.

Data supplements

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Bacteria appear to mediate hyena social odors
Kevin R. Theis, Arvind Venkataraman, Jacquelyn A. Dycus, Keith D. Koonter, Emily N. Schmitt-Matzen, Aaron P. Wagner, Kay E. Holekamp, Thomas M. Schmidt
Proceedings of the National Academy of Sciences Dec 2013, 110 (49) 19832-19837; DOI: 10.1073/pnas.1306477110

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Bacteria appear to mediate hyena social odors
Kevin R. Theis, Arvind Venkataraman, Jacquelyn A. Dycus, Keith D. Koonter, Emily N. Schmitt-Matzen, Aaron P. Wagner, Kay E. Holekamp, Thomas M. Schmidt
Proceedings of the National Academy of Sciences Dec 2013, 110 (49) 19832-19837; DOI: 10.1073/pnas.1306477110
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