Evolutionary trends in host physiology outweigh dietary niche in structuring primate gut microbiomes

Katherine R. Amato, Jon G. Sanders, Se Jin Song, Michael Nute, Jessica L. Metcalf, Luke R. Thompson, James T. Morton, Amnon Amir, Valerie J. McKenzie, Gregory Humphrey, Grant Gogul, James Gaffney, Andrea L. Baden, Gillian A.O. Britton, Frank P. Cuozzo, Anthony Di Fiore, Nathaniel J. Dominy, Tony L. Goldberg, Andres Gomez, Martin M. KowalewskiRebecca J. Lewis, Andres Link, Michelle L. Sauther, Stacey Tecot, Bryan A. White, Karen E. Nelson, Rebecca M. Stumpf, Rob Knight, Steven R. Leigh

Research output: Contribution to journalArticlepeer-review

64 Scopus citations

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 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.

Original languageEnglish (US)
Pages (from-to)576-587
Number of pages12
JournalISME Journal
Volume13
Issue number3
DOIs
StatePublished - Mar 1 2019

Bibliographical note

Funding Information:
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 Micro-biome). 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.

Publisher Copyright:
© 2018, International Society for Microbial Ecology.

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