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

Publication 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

  • 10,702
    Page views
  • 1,961
    Downloads
  • 273
    Citations

Article citation count generated by polling the highest count across the following sources: Scopus, Crossref, PubMed Central.

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

Further reading

    1. Ecology
    2. Evolutionary Biology
    Nicholas M Grebe, Jean Paul Hirwa ... Stacy Rosenbaum
    Research Article Updated

    Evolutionary theories predict that sibling relationships will reflect a complex balance of cooperative and competitive dynamics. In most mammals, dispersal and death patterns mean that sibling relationships occur in a relatively narrow window during development and/or only with same-sex individuals. Besides humans, one notable exception is mountain gorillas, in which non-sex-biased dispersal, relatively stable group composition, and the long reproductive tenures of alpha males mean that animals routinely reside with both maternally and paternally related siblings, of the same and opposite sex, throughout their lives. Using nearly 40,000 hr of behavioral data collected over 14 years on 699 sibling and 1235 non-sibling pairs of wild mountain gorillas, we demonstrate that individuals have strong affiliative preferences for full and maternal siblings over paternal siblings or unrelated animals, consistent with an inability to discriminate paternal kin. Intriguingly, however, aggression data imply the opposite. Aggression rates were statistically indistinguishable among all types of dyads except one: in mixed-sex dyads, non-siblings engaged in substantially more aggression than siblings of any type. This pattern suggests mountain gorillas may be capable of distinguishing paternal kin but nonetheless choose not to affiliate with them over non-kin. We observe a preference for maternal kin in a species with a high reproductive skew (i.e. high relatedness certainty), even though low reproductive skew (i.e. low relatedness certainty) is believed to underlie such biases in other non-human primates. Our results call into question reasons for strong maternal kin biases when paternal kin are identifiable, familiar, and similarly likely to be long-term groupmates, and they may also suggest behavioral mismatches at play during a transitional period in mountain gorilla society.

    1. Ecology
    2. Evolutionary Biology
    Dakota E McCoy, Benjamin Goulet-Scott ... John Kartesz
    Tools and Resources

    Sustainable cities depend on urban forests. City trees-pillars of urban forests - improve our health, clean the air, store CO2, and cool local temperatures. Comparatively less is known about city tree communities as ecosystems, particularly regarding spatial composition, species diversity, tree health, and the abundance of introduced species. Here, we assembled and standardized a new dataset of N=5,660,237 trees from 63 of the largest US cities with detailed information on location, health, species, and whether a species is introduced or naturally occurring (i.e., 'native'). We further designed new tools to analyze spatial clustering and the abundance of introduced species. We show that trees significantly cluster by species in 98% of cities, potentially increasing pest vulnerability (even in species-diverse cities). Further, introduced species significantly homogenize tree communities across cities, while naturally occurring trees (i.e., 'native' trees) comprise 0.51%-87.3% (median=45.6%) of city tree populations. Introduced species are more common in drier cities, and climate also shapes tree species diversity across urban forests. Parks have greater tree species diversity than urban settings. Compared to past work which focused on canopy cover and species richness, we show the importance of analyzing spatial composition and introduced species in urban ecosystems (and we develop new tools and datasets to do so). Future work could analyze city trees and socio-demographic variables or bird, insect, and plant diversity (e.g., from citizen-science initiatives). With these tools, we may evaluate existing city trees in new, nuanced ways and design future plantings to maximize resistance to pests and climate change. We depend on city trees.