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The evolution of the host microbiome as an ecosystem on a leash

Nature volume 548, pages 4351 (03 August 2017) | Download Citation

Abstract

The human body carries vast communities of microbes that provide many benefits. Our microbiome is complex and challenging to understand, but evolutionary theory provides a universal framework with which to analyse its biology and health impacts. Here we argue that to understand a given microbiome feature, such as colonization resistance, host nutrition or immune development, we must consider how hosts and symbionts evolve. Symbionts commonly evolve to compete within the host ecosystem, while hosts evolve to keep the ecosystem on a leash. We suggest that the health benefits of the microbiome should be understood, and studied, as an interplay between microbial competition and host control.

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Acknowledgements

We thank J. Boomsma, J. Thompson, S. Knowles and N. Ruby for discussions and comments on the manuscript, and D. Hughes, A. Wilson, M. McFall-Ngai for providing images for Fig. 2. K.R.F. is funded by European Research Council grant 242670 and a Calleva Research Centre for Evolution and Human Science (Magdalen College, Oxford) grant. K.Z.C. is funded by a Sir Henry Wellcome Postdoctoral Research Fellowship (grant 201341/Z/16/Z). J.S. is funded by an NIH grant to E. Pamer and J. Xavier (project number 1U01AI124275-01). S.R.-N. is funded by NIH grant 1K08AI130392-01 and a Career Award for Medical Scientists from the Burroughs Wellcome Fund.

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Affiliations

  1. Department of Zoology, University of Oxford, Oxford OX1 3PS, UK

    • Kevin R. Foster
    •  & Katharine Z. Coyte
  2. Computational Biology Program, Memorial Sloan Kettering Cancer Center, New York, New York 10065, USA

    • Jonas Schluter
    •  & Katharine Z. Coyte
  3. Division of Infectious Diseases and Division of Gastroenterology, Department of Medicine, Boston Children’s Hospital and Harvard Medical School, 300 Longwood Avenue, Boston, Massachusetts 02115, USA

    • Katharine Z. Coyte
    •  & Seth Rakoff-Nahoum

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All authors contributed to the planning and writing of the manuscript.

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The authors declare no competing financial interests.

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Correspondence to Kevin R. Foster or Seth Rakoff-Nahoum.

Reviewer Information Nature thanks S. Brown, D. A. Relman and the other anonymous reviewer(s) for their contribution to the peer review of this work.

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