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

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.

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.

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

Computational Biology Program, Memorial Sloan Kettering Cancer Center, New York, 10065, New York, USA

Division of Infectious Diseases and Division of Gastroenterology, Department of Medicine, Boston Children’s Hospital and Harvard Medical School, 300 Longwood Avenue, Boston, 02115,

Massachusetts, USA

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

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.

Publisher's note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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The microbial communities that inhabit the human body provide several benefits to their host, but the evolutionary basis of this complex relationship is unclear. In this Perspective, Kevin

Foster and colleagues propose an evolutionary framework for understanding the dynamics of the microbiome. They argue that, in order to understand the microbiome and harness it for health

benefits, we need to view the relationship between host and symbiont as one based on microbial competition and host control.