Abstract

Microbiomes impact a variety of processes including a host’s ability to access nutrients and maintain health. While host species differences in microbiomes have been described across ecosystems, little is known about how microbiomes assemble, particularly in the ecological and social contexts in which they evolved. We examined gut microbiome composition in nine sympatric wild non-human primate (NHP) species. Despite sharing an environment and interspecific interactions, individuals harbored unique and persistent microbiomes influenced by host species, social group, and parentage, but surprisingly not by social relationships among members of a social group. We found a branching order of host-species networks constructed using the composition of their microbiomes as characters, which was incongruent with known NHP phylogenetic relationships, with chimpanzees (Pan troglodytes verus) sister to colobines, upon which they regularly prey. In contrast to phylogenetic clustering found in all monkey microbiomes, chimpanzee microbiomes were unique in that they exhibited patterns of phylogenetic overdispersion. This reflects unique ecological processes impacting microbiome composition in chimpanzees and future studies will elucidate the aspects of chimpanzee ecology, life history, and physiology that explain their unique microbiome community structure. Our study of contemporaneous microbiomes of all sympatric diurnal NHP in an ecosystem highlights the diverse dispersal routes shaping these complex communities.

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Acknowledgements

This article represents a chapter in the doctoral dissertation of J.F.G. and benefited greatly from the input of his supervision committee, David Marcogliese, Charles Nunn, and Louis Lefebvre. We are grateful to the Ivorian Ministry of Research, the Ivorian Ministry of Environment and Forests, as well as the Office Ivoirien des Parcs et Réserves for giving permission to conduct this study. We thank the directorship of the Taï National Park, the Centre Suisse de Recherche Scientifique, the Taï Chimpanzee Project and their teams of field assistants for their support. J.F.G. was supported by an NSF Graduate Research Fellowship (DGE-1142336), the Canadian Institutes of Health Research’s Strategic Training Initiative in Health Research’s Systems Biology Training Program, an NSERC Vanier Canada Graduate Scholarship (CGS), and a long-term Research Grant from the German Academic Exchange Service (DAAD-91525837-57048249). Core-funding for the Taï Chimpanzee Project is provided by the Max Planck Society. This research also benefited from discussions within the Deutsche Forschungsgemeinschaft (DFG) research group “Sociality and Health in Primates” (FOR2136). For assistance in the field we thank Ariane Düx, Vera Leinert, Bekah Myers, Jonathan Müller-Tiburtius, Sylvain Lemoine, and the long-term mangabey field assistants Simon T. Kannieu, Daniel Bouin, and Gnimion Florent. For assistance and support with sequencing at the Microbial Analysis and Services Facility at the University of Connecticut we are grateful to Kendra Maas. For their support in the laboratory, J.F.G. thanks Ulla Thiesen, Kevin Merkel, Andreas Sachse, and the P3 group at the Robert Koch Institute. J.F.G. thanks James Herrera and Will Pearse for discussions and sharing R code for phylogenetic analyses.

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Author notes

  1. These authors contributed equally: Fabian H. Leendertz, Sébastien Calvignac-Spencer.

Affiliations

  1. Department of Biology, McGill University, 855 Sherbrooke Street West, Montreal, QC, H3A2T7, Canada

    • Jan F. Gogarten
    •  & T. Jonathan Davies
  2. Primatology Department, Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, 04103, Leipzig, Germany

    • Jan F. Gogarten
    • , Alexander Mielke
    •  & Roman M. Wittig
  3. Project Group Epidemiology of Highly Pathogenic Microorganisms, Robert Koch Institute, Seestraße 10, 13353, Berlin, Germany

    • Jan F. Gogarten
    • , Fabian H. Leendertz
    •  & Sébastien Calvignac-Spencer
  4. Department of Molecular and Cell Biology, University of Connecticut, 91 North Eagleville Road, Unit 3125, Storrs, CT, 06269-3125, USA

    • Jacquelynn Benjamino
    • , J. Peter Gogarten
    • , Joerg Graf
    •  & Michael C. Nelson
  5. Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, 04103, Leipzig, Germany

    • Roger Mundry
  6. Taï Chimpanzee Project, Centre Suisse de Recherches Scientifiques, B.P. 1303, Abidjan 01, Côte d’Ivoire

    • Roman M. Wittig

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Correspondence to Roman M. Wittig or Fabian H. Leendertz or Sébastien Calvignac-Spencer.

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https://doi.org/10.1038/s41396-018-0166-1