Social networks predict gut microbiome composition in wild baboons

  1. Jenny Tung
  2. Luis B Barreiro
  3. Michael B Burns
  4. Jean-Christophe Grenier
  5. Josh Lynch
  6. Laura E Grieneisen
  7. Jeanne Altmann
  8. Susan C Alberts
  9. Ran Blekhman
  10. Elizabeth A Archie  Is a corresponding author
  1. Duke University, United States
  2. University of Montreal, Canada
  3. University of Minnesota, United States
  4. University of Notre Dame, United States
  5. National Museums of Kenya, Kenya

Abstract

Social relationships have profound effects on health in humans and other primates, but the mechanisms that explain this relationship are not well understood. Using shotgun metagenomic data from wild baboons, we found that social group membership and social network relationships predicted both the taxonomic structure of the gut microbiome and the structure of genes encoded by gut microbial species. Rates of interaction directly explained variation in the gut microbiome, even after controlling for diet, kinship, and shared environments. They therefore strongly implicate direct physical contact among social partners in the transmission of gut microbial species. We identified 51 socially structured taxa, which were significantly enriched for anaerobic and non-spore-forming lifestyles. Our results argue that social interactions are an important determinant of gut microbiome composition in natural animal populations-a relationship with important ramifications for understanding how social relationships influence health, as well as the evolution of group living.

Article and author information

Author details

  1. Jenny Tung

    Department of Evolutionary Anthropology, Duke University, Durham, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Luis B Barreiro

    Department of Pediatrics, Sainte-Justine Hospital Research Centre, University of Montreal, Montreal, Canada
    Competing interests
    The authors declare that no competing interests exist.
  3. Michael B Burns

    Department of Genetics, Cell Biology, and Development, University of Minnesota, Minneapolis, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Jean-Christophe Grenier

    Department of Pediatrics, Sainte-Justine Hospital Research Centre, University of Montreal, Montreal, Canada
    Competing interests
    The authors declare that no competing interests exist.
  5. Josh Lynch

    Department of Genetics, Cell Biology, and Development; Department of Ecology, Evolution, and Behavior, University of Minnesota, Minneapolis, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Laura E Grieneisen

    Department of Biological Sciences, University of Notre Dame, Notre Dame, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Jeanne Altmann

    Institute of Primate Research, National Museums of Kenya, Nairobi, Kenya
    Competing interests
    The authors declare that no competing interests exist.
  8. Susan C Alberts

    Department of Biology, Duke University, Durham, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Ran Blekhman

    Department of Genetics, Cell Biology, and Development, University of Minnesota, Minneapolis, United States
    Competing interests
    The authors declare that no competing interests exist.
  10. Elizabeth A Archie

    Institute of Primate Research, National Museums of Kenya, Nairobi, Kenya
    For correspondence
    earchie@nd.edu
    Competing interests
    The authors declare that no competing interests exist.

Copyright

© 2015, Tung et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 11,407
    views
  • 2,176
    downloads
  • 384
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Jenny Tung
  2. Luis B Barreiro
  3. Michael B Burns
  4. Jean-Christophe Grenier
  5. Josh Lynch
  6. Laura E Grieneisen
  7. Jeanne Altmann
  8. Susan C Alberts
  9. Ran Blekhman
  10. Elizabeth A Archie
(2015)
Social networks predict gut microbiome composition in wild baboons
eLife 4:e05224.
https://doi.org/10.7554/eLife.05224

Share this article

https://doi.org/10.7554/eLife.05224

Further reading

    1. Ecology
    Itai Bloch, David Troupin ... Nir Sapir
    Research Article

    Optimal foraging theory posits that foragers adjust their movements based on prey abundance to optimize food intake. While extensively studied in terrestrial and marine environments, aerial foraging has remained relatively unexplored due to technological limitations. This study, uniquely combining BirdScan-MR1 radar and the Advanced Tracking and Localization of Animals in Real-Life Systems biotelemetry system, investigates the foraging dynamics of Little Swifts (Apus affinis) in response to insect movements over Israel’s Hula Valley. Insect movement traffic rate (MoTR) substantially varied across days, strongly influencing swift movement. On days with high MoTR, swifts exhibited reduced flight distance, increased colony visit rate, and earlier arrivals at the breeding colony, reflecting a dynamic response to prey availability. However, no significant effects were observed in total foraging duration, flight speed, or daily route length. Notably, as insect abundance increased, inter-individual distances decreased. These findings suggest that Little Swifts optimize their foraging behavior in relation to aerial insect abundance, likely influencing reproductive success and population dynamics. The integration of radar technology and biotelemetry systems provides a unique perspective on the interactions between aerial insectivores and their prey, contributing to a comprehensive understanding of optimal foraging strategies in diverse environments.

    1. Ecology
    2. Evolutionary Biology
    Rebecca D Tarvin, Jeffrey L Coleman ... Richard W Fitch
    Research Article

    Understanding the origins of novel, complex phenotypes is a major goal in evolutionary biology. Poison frogs of the family Dendrobatidae have evolved the novel ability to acquire alkaloids from their diet for chemical defense at least three times. However, taxon sampling for alkaloids has been biased towards colorful species, without similar attention paid to inconspicuous ones that are often assumed to be undefended. As a result, our understanding of how chemical defense evolved in this group is incomplete. Here, we provide new data showing that, in contrast to previous studies, species from each undefended poison frog clade have measurable yet low amounts of alkaloids. We confirm that undefended dendrobatids regularly consume mites and ants, which are known sources of alkaloids. Thus, our data suggest that diet is insufficient to explain the defended phenotype. Our data support the existence of a phenotypic intermediate between toxin consumption and sequestration — passive accumulation — that differs from sequestration in that it involves no derived forms of transport and storage mechanisms yet results in low levels of toxin accumulation. We discuss the concept of passive accumulation and its potential role in the origin of chemical defenses in poison frogs and other toxin-sequestering organisms. In light of ideas from pharmacokinetics, we incorporate new and old data from poison frogs into an evolutionary model that could help explain the origins of acquired chemical defenses in animals and provide insight into the molecular processes that govern the fate of ingested toxins.