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The microbiome beyond the horizon of ecological and evolutionary theory

Abstract

The ecological and evolutionary study of community formation, diversity, and stability is rooted in general theory and reinforced by decades of system-specific empirical work. Deploying these ideas to study the assembly, complexity, and dynamics of microbial communities living in and on eukaryotes has proved seductive, but challenging. The success of this research endeavour depends on our capacity to observe and characterize the distributions, abundances, and functional traits of microbiota, representing an array of technical and analytical challenges. Furthermore, a number of unique characteristics of microbial species, such as horizontal gene transfer, the production of public goods, toxin and antibiotic production, rapid evolution, and feedbacks between the microbiome and its host, are not easily accommodated by current ecological and evolutionary theory. Here we highlight potential pitfalls in the application of existing theoretical tools without careful consideration of the unique complexities of the microbiome, focusing particularly on the issue of human health, and anchoring our discussion in existing empirical evidence.

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Fig. 1: Illustration of the various -omics approaches and the advantages of combining methods to understand microbiome function.
Fig. 2: Evolutionary and ecological principles influencing microbiome establishment, stability, and transmission among generations.

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Acknowledgements

We thank the RAPIDD program of the Science & Technology Directorate, Department of Homeland Security and the Fogarty International Center, National Institutes of Health and Wellcome Trust for funding the workshop from which this manuscript emerged, and all workshop participants (M. Blaser; S. Brown; A. Buckling; S. Chen; D. Churamani; M. Claesson; W. Cookson; M. Cox; K. Coyte; J. Curtis; K. Davies; R. De Weirdt; J. Dore; S. D. Ehrlich; M. Ferguson; H. Flint; K. Foster; B. Grenfell; N. Ilott; A. Johnson; A. Kuspa; R. La Ragione; T. Lawley; S. Levin; J. M. Welch; K. Moses; J. Parkhill; P Rainey; J. Segre; D. Spratt; C. Steves; Z. Takats; C. Tropini; M. Tunney; A. Wallace; A. Watson; D. Weinkove; C. Weller; P. Wilmes; N. Wingreen; J. Xavier); as well as organizers, D. Cannon and A. Cave,for further discussion of the manuscript.

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B.K., L.J.H. and C.J.E.M. all contributed to the formation of ideas and writing of this manuscript.

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Correspondence to Britt Koskella.

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Koskella, B., Hall, L.J. & Metcalf, C.J.E. The microbiome beyond the horizon of ecological and evolutionary theory. Nat Ecol Evol 1, 1606–1615 (2017). https://doi.org/10.1038/s41559-017-0340-2

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