Abstract

Over the past decade several studies have reported that the gut microbiomes of mammals with similar dietary niches exhibit similar compositional and functional traits. However, these studies rely heavily on samples from captive individuals and often confound host phylogeny, gut morphology, and diet. To more explicitly test the influence of host dietary niche on the mammalian gut microbiome we use 16S rRNA gene amplicon sequencing and shotgun metagenomics to compare the gut microbiota of 18 species of wild non-human primates classified as either folivores or closely related non-folivores, evenly distributed throughout the primate order and representing a range of gut morphological specializations. While folivory results in some convergent microbial traits, collectively we show that the influence of host phylogeny on both gut microbial composition and function is much stronger than that of host dietary niche. This pattern does not result from differences in host geographic location or actual dietary intake at the time of sampling, but instead appears to result from of differences in host physiology. These findings indicate that mammalian gut microbiome plasticity in response to dietary shifts over both the lifespan of an individual host and the evolutionary history of a given host species is constrained by host physiological evolution. Therefore, the gut microbiome cannot be considered separately from host physiology when describing host nutritional strategies and the emergence of host dietary niches.

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Acknowledgements

This project was funded by the NSF (HOMINID, grant #0935347), the Earth Microbiome Project (W.M. Keck Foundation DT061413), and the John Templeton Foundation (Grant ID 44000, Convergent Evolution of the Vertebrate Microbiome). Field collection of samples was funded through a variety of individual grants awarded to the co-authors and collaborators listed in Table S1. The authors are grateful for the support with logistics and permits provided by the US government, as well as the governments and local agencies associated with each nation listed in Table S1, as well as countless field assistants at these locations. Raw sequence data generated by 16S rRNA amplicon sequencing and shotgun metagenomics are located in EBI under accession ERP104379.

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Affiliations

  1. Department of Anthropology, Northwestern University, Evanston, USA

    • Katherine R. Amato
  2. Department of Pediatrics, University of California San Diego, San Diego, USA

    • Jon G. Sanders
    • , Se Jin Song
    • , Luke R. Thompson
    • , James T. Morton
    • , Amnon Amir
    • , Gregory Humphrey
    •  & Rob Knight
  3. Department of Statistics, University of Illinois at Urbana-Champaign, Urbana, USA

    • Michael Nute
  4. Department of Animal Sciences, Colorado State University, Fort Collins, USA

    • Jessica L. Metcalf
  5. Center for Microbiome Research, University of California San Diego, San Diego, USA

    • Jon G. Sanders
    • , Se Jin Song
    • , Luke R. Thompson
    • , James T. Morton
    • , Amnon Amir
    • , Gregory Humphrey
    •  & Rob Knight
  6. Department of Ecology and Evolutionary Biology, University of Colorado Boulder, Boulder, USA

    • Valerie J. McKenzie
  7. BioFrontiers Institute, University of Colorado Boulder, Boulder, USA

    • Grant Gogul
    •  & James Gaffney
  8. Department of Anthropology, Hunter College of City University of New York, New York, USA

    • Andrea L. Baden
  9. Department of Anthropology, Dartmouth College, Hanover, USA

    • Gillian A.O. Britton
    •  & Nathaniel J. Dominy
  10. Lajuma Research Centre, Louis Trichardt (Makhado), South Africa

    • Frank P. Cuozzo
  11. Department of Anthropology, University of Texas Austin, Austin, USA

    • Anthony Di Fiore
    •  & Rebecca J. Lewis
  12. Department of Pathobiological Sciences, University of Wisconsin-Madison, Madison, USA

    • Tony L. Goldberg
  13. Department of Animal Sciences, University of Minnesota, Minneapolis, USA

    • Andres Gomez
  14. Estacion Biologica Corrientes (MACN-BR) – CONICET, Corrientes, Argentina

    • Martin M. Kowalewski
  15. Department of Biological Sciences and School of Management, Universidad de los Andes, Bogota, Colombia

    • Andres Link
  16. Department of Anthropology, University of Colorado Boulder, Boulder, USA

    • Michelle L. Sauther
    •  & Steven R. Leigh
  17. School of Anthropology, University of Arizona, Tucson, USA

    • Stacey Tecot
  18. Department of Animal Sciences, University of Illinois at Urbana-Champaign, Urbana, USA

    • Bryan A. White
  19. Departments of Human Biology and Genomic Medicine, J. Craig Venter Institute, La Jolla, CA, 92037, USA

    • Karen E. Nelson
  20. Department of Anthropology, University of Illinois at Urbana-Champaign, Urbana, USA

    • Rebecca M. Stumpf
  21. Department of Computer Science and Engineering, University of California San Diego, San Diego, USA

    • James T. Morton
    •  & Rob Knight

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The authors declare that they have no conflict of interest.

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Correspondence to Katherine R. Amato.

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DOI

https://doi.org/10.1038/s41396-018-0175-0

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