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.

Reviewing Editor

  1. Eric Alm, MIT, United States

Version history

  1. Received: October 17, 2014
  2. Accepted: February 27, 2015
  3. Accepted Manuscript published: March 16, 2015 (version 1)
  4. Version of Record published: March 31, 2015 (version 2)

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

  • 11,181
    views
  • 2,080
    downloads
  • 324
    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
    Anna L Erdei, Aneth B David ... Teun Dekker
    Research Article Updated

    Over two decades ago, an intercropping strategy was developed that received critical acclaim for synergizing food security with ecosystem resilience in smallholder farming. The push–pull strategy reportedly suppresses lepidopteran pests in maize through a combination of a repellent intercrop (push), commonly Desmodium spp., and an attractive, border crop (pull). Key in the system is the intercrop’s constitutive release of volatile terpenoids that repel herbivores. However, the earlier described volatile terpenoids were not detectable in the headspace of Desmodium, and only minimally upon herbivory. This was independent of soil type, microbiome composition, and whether collections were made in the laboratory or in the field. Furthermore, in oviposition choice tests in a wind tunnel, maize with or without an odor background of Desmodium was equally attractive for the invasive pest Spodoptera frugiperda. In search of an alternative mechanism, we found that neonate larvae strongly preferred Desmodium over maize. However, their development stagnated and no larva survived. In addition, older larvae were frequently seen impaled and immobilized by the dense network of silica-fortified, non-glandular trichomes. Thus, our data suggest that Desmodium may act through intercepting and decimating dispersing larval offspring rather than adult deterrence. As a hallmark of sustainable pest control, maize–Desmodium push–pull intercropping has inspired countless efforts to emulate stimulo-deterrent diversion in other cropping systems. However, detailed knowledge of the actual mechanisms is required to rationally improve the strategy, and translate the concept to other cropping systems.

    1. Ecology
    Songdou Zhang, Shiheng An
    Insight

    The bacterium responsible for a disease that infects citrus plants across Asia facilitates its own proliferation by increasing the fecundity of its host insect.