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

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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Figure 1: Convergent evolution of the host epithelial interface with the microbiota.
Figure 2: Models of host–microbiome interaction.

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References

  1. Costello, E. K., Stagaman, K., Dethlefsen, L., Bohannan, B. J. & Relman, D. A. The application of ecological theory toward an understanding of the human microbiome. Science 336, 1255–1262 (2012)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  2. The Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature 486, 207–214 (2012)

  3. Hacquard, S. et al. Microbiota and host nutrition across plant and animal kingdoms. Cell Host Microbe 17, 603–616 (2015)

    Article  CAS  PubMed  Google Scholar 

  4. Hooper, L. V., Littman, D. R. & Macpherson, A. J. Interactions between the microbiota and the immune system. Science 336, 1268–1273 (2012)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  5. van der Waaij, D., Berghuis-de Vries, J. M. & Lekkerkerk-van der Wees, J. E. C. Colonization resistance of the digestive tract in conventional and antibiotic-treated mice. J. Hyg. (Lond.) 69, 405–411 (1971)

    Article  CAS  Google Scholar 

  6. Buffie, C. G. et al. Precision microbiome reconstitution restores bile acid mediated resistance to Clostridium difficile. Nature 517, 205–208 (2015)

    Article  ADS  CAS  PubMed  Google Scholar 

  7. Cryan, J. F. & Dinan, T. G. Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat. Rev. Neurosci. 13, 701–712 (2012)

    Article  CAS  PubMed  Google Scholar 

  8. Marchesi, J. R. & Ravel, J. The vocabulary of microbiome research: a proposal. Microbiome 3, 31 (2015)

    Article  PubMed  PubMed Central  Google Scholar 

  9. Nadell, C. D., Drescher, K. & Foster, K. R. Spatial structure, cooperation and competition in biofilms. Nat. Rev. Microbiol. 14, 589–600 (2016)

    Article  CAS  PubMed  Google Scholar 

  10. Chatzidaki-Livanis, M., Geva-Zatorsky, N. & Comstock, L. E. Bacteroides fragilis type VI secretion systems use novel effector and immunity proteins to antagonize human gut Bacteroidales species. Proc. Natl Acad. Sci. USA 113, 3627–3632 (2016)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  11. Kommineni, S. et al. Bacteriocin production augments niche competition by enterococci in the mammalian gastrointestinal tract. Nature 526, 719–722 (2015)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  12. Wexler, A. G. et al. Human symbionts inject and neutralize antibacterial toxins to persist in the gut. Proc. Natl Acad. Sci. USA 113, 3639–3644 (2016)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  13. Rakoff-Nahoum, S., Foster, K. R. & Comstock, L. E. The evolution of cooperation within the gut microbiota. Nature 533, 255–259 (2016)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  14. Coyte, K. Z., Schluter, J. & Foster, K. R. The ecology of the microbiome: networks, competition, and stability. Science 350, 663–666 (2015)

    Article  ADS  CAS  PubMed  Google Scholar 

  15. Stein, R. R. et al. Ecological modeling from time-series inference: insight into dynamics and stability of intestinal microbiota. PLoS Comput. Biol. 9, e1003388 (2013). Using ecological models fitted to data, this landmark study estimates ecological interactions within the microbiota and concludes there is a lot of competition and exploitation

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  16. Lozupone, C. A., Stombaugh, J. I., Gordon, J. I., Jansson, J. K. & Knight, R. Diversity, stability and resilience of the human gut microbiota. Nature 489, 220–230 (2012)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  17. Ley, R. E., Lozupone, C. A., Hamady, M., Knight, R. & Gordon, J. I. Worlds within worlds: evolution of the vertebrate gut microbiota. Nat. Rev. Microbiol. 6, 776–788 (2008)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. De Mazancourt, C., Loreau, M. & Dieckmann, U. Understanding mutualism when there is adaptation to the partner. J. Ecol. 93, 305–314 (2005)

    Article  Google Scholar 

  19. Mushegian, A. A. & Ebert, D. Rethinking “mutualism” in diverse host–symbiont communities. BioEssays 38, 100–108 (2016)

    Article  PubMed  Google Scholar 

  20. Foster, K. R. & Wenseleers, T. A general model for the evolution of mutualisms. J. Evol. Biol. 19, 1283–1293 (2006)

    Article  CAS  PubMed  Google Scholar 

  21. West, S. A., Kiers, E. T., Simms, E. L. & Denison, R. F. Sanctions and mutualism stability: why do rhizobia fix nitrogen? Proc. R. Soc. B 269, 685–694 (2002)

    PubMed  Google Scholar 

  22. Schluter, J. & Foster, K. R. The evolution of mutualism in gut microbiota via host epithelial selection. PLoS Biol. 10, e1001424 (2012). Theoretical study predicting the importance of host control in the microbiome

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Douglas, A. E. & Werren, J. H. Holes in the hologenome: why host–microbe symbioses are not holobionts. MBio 7, e02099–15 (2016). Critical analysis of the holobiont concept

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Bordenstein, S. R. & Theis, K. R. Host biology in light of the microbiome: ten principles of holobionts and hologenomes. PLoS Biol. 13, e1002226 (2015)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  25. Rivera-Chávez, F. & Bäumler, A. J. The pyromaniac inside you: Salmonella metabolism in the host gut. Annu. Rev. Microbiol. 69, 31–48 (2015)

    Article  PubMed  CAS  Google Scholar 

  26. Darwin, C. R. On the Origin of Species by Means of Natural Selection or the Preservation of Favoured Races in the Struggle for Life (Murray, 1859)

  27. Janzen, D. H. Coevolution of mutualism between ants and acacias in Central America. Evolution 20, 249–275 (1966)

    Article  PubMed  Google Scholar 

  28. Scheuring, I. & Yu, D. W. How to assemble a beneficial microbiome in three easy steps. Ecol. Lett. 15, 1300–1307 (2012)

    Article  PubMed  PubMed Central  Google Scholar 

  29. Welzl, H., D’Adamo, P. & Lipp, H.-P. Conditioned taste aversion as a learning and memory paradigm. Behav. Brain Res. 125, 205–213 (2001)

    Article  CAS  PubMed  Google Scholar 

  30. Imhann, F. et al. Proton pump inhibitors affect the gut microbiome. Gut 65, 740–748 (2016)

    Article  CAS  PubMed  Google Scholar 

  31. Poulsen, M. & Boomsma, J. J. Mutualistic fungi control crop diversity in fungus-growing ants. Science 307, 741–744 (2005)

    Article  ADS  CAS  PubMed  Google Scholar 

  32. Kaltenpoth, M. et al. Partner choice and fidelity stabilize coevolution in a Cretaceous-age defensive symbiosis. Proc. Natl Acad. Sci. USA 111, 6359–6364 (2014)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  33. Bokulich, N. A. et al. Antibiotics, birth mode, and diet shape microbiome maturation during early life. Sci. Transl. Med. 8, 343ra382 (2016)

    Article  CAS  Google Scholar 

  34. LoCascio, R. G. et al. Glycoprofiling of bifidobacterial consumption of human milk oligosaccharides demonstrates strain specific, preferential consumption of small chain glycans secreted in early human lactation. J. Agric. Food Chem. 55, 8914–8919 (2007)

    Article  CAS  PubMed  Google Scholar 

  35. Caldara, M. et al. Mucin biopolymers prevent bacterial aggregation by retaining cells in the free-swimming state. Curr. Biol. 22, 2325–2330 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Philippot, L., Raaijmakers, J. M., Lemanceau, P. & van der Putten, W. H. Going back to the roots: the microbial ecology of the rhizosphere. Nat. Rev. Microbiol. 11, 789–799 (2013)

    Article  CAS  PubMed  Google Scholar 

  37. Jones, D. L., Nguyen, C. & Finlay, R. D. Carbon flow in the rhizosphere: carbon trading at the soil–root interface. Plant Soil 321, 5–33 (2009)

    Article  CAS  Google Scholar 

  38. Vaishnava, S. et al. The antibacterial lectin RegIIIγ promotes the spatial segregation of microbiota and host in the intestine. Science 334, 255–258 (2011)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  39. Okumura, R. et al. Lypd8 promotes the segregation of flagellated microbiota and colonic epithelia. Nature 532, 117–121 (2016)

    Article  ADS  CAS  PubMed  Google Scholar 

  40. Rakoff-Nahoum, S., Paglino, J., Eslami-Varzaneh, F., Edberg, S. & Medzhitov, R. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 118, 229–241 (2004)

    Article  CAS  PubMed  Google Scholar 

  41. Franzenburg, S. et al. MyD88-deficient Hydra reveal an ancient function of TLR signaling in sensing bacterial colonizers. Proc. Natl Acad. Sci. USA 109, 19374–19379 (2012). Evidence of an ancient role for the immune system in regulation of the microbiota

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  42. Barton, G. M. & Kagan, J. C. A cell biological view of Toll-like receptor function: regulation through compartmentalization. Nat. Rev. Immunol. 9, 535–542 (2009)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Lamkanfi, M. & Dixit, V. M. Mechanisms and functions of inflammasomes. Cell 157, 1013–1022 (2014)

    Article  CAS  PubMed  Google Scholar 

  44. Xu, H. et al. Innate immune sensing of bacterial modifications of Rho GTPases by the Pyrin inflammasome. Nature 513, 237–241 (2014)

    Article  ADS  CAS  PubMed  Google Scholar 

  45. Jones, J. D. & Dangl, J. L. The plant immune system. Nature 444, 323–329 (2006)

    Article  ADS  CAS  PubMed  Google Scholar 

  46. Kiers, E. T., Rousseau, R. A., West, S. A. & Denison, R. F. Host sanctions and the legume–rhizobium mutualism. Nature 425, 78–81 (2003). Evidence of powerful host control from plants

    Article  ADS  CAS  PubMed  Google Scholar 

  47. Roediger, W. E. Role of anaerobic bacteria in the metabolic welfare of the colonic mucosa in man. Gut 21, 793–798 (1980)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Arpaia, N. & Rudensky, A. Y. Microbial metabolites control gut inflammatory responses. Proc. Natl Acad. Sci. USA 111, 2058–2059 (2014)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  49. Barroso-Batista, J., Demengeot, J. & Gordo, I. Adaptive immunity increases the pace and predictability of evolutionary change in commensal gut bacteria. Nat. Commun. 6, 8945 (2015)

    Article  ADS  CAS  PubMed  Google Scholar 

  50. Foster, K. R. The sociobiology of molecular systems. Nat. Rev. Genet. 12, 193–203 (2011)

    Article  CAS  PubMed  Google Scholar 

  51. Kato, L. M., Kawamoto, S., Maruya, M. & Fagarasan, S. The role of the adaptive immune system in regulation of gut microbiota. Immunol. Rev. 260, 67–75 (2014)

    Article  CAS  PubMed  Google Scholar 

  52. Sonnenburg, J. L. et al. Glycan foraging in vivo by an intestine-adapted bacterial symbiont. Science 307, 1955–1959 (2005)

    Article  ADS  CAS  PubMed  Google Scholar 

  53. Brown, B. E. & Bythell, J. C. Perspectives on mucus secretion in reef corals. Mar. Ecol. Prog. Ser. 296, 291–309 (2005)

    Article  ADS  CAS  Google Scholar 

  54. Glasl, B., Herndl, G. J. & Frade, P. R. The microbiome of coral surface mucus has a key role in mediating holobiont health and survival upon disturbance. ISME J. 10, 2280–2292 (2016)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Nguema-Ona, E., Vicré-Gibouin, M., Cannesan, M.-A. & Driouich, A. Arabinogalactan proteins in root–microbe interactions. Trends Plant Sci. 18, 440–449 (2013)

    Article  CAS  PubMed  Google Scholar 

  56. McLoughlin, K., Schluter, J., Rakoff-Nahoum, S., Smith, A. L. & Foster, K. R. Host selection of microbiota via differential adhesion. Cell Host Microbe 19, 550–559 (2016)

    Article  CAS  PubMed  Google Scholar 

  57. Huang, J. Y., Lee, S. M. & Mazmanian, S. K. The human commensal Bacteroides fragilis binds intestinal mucin. Anaerobe 17, 137–141 (2011)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Hibbing, M. E., Fuqua, C., Parsek, M. R. & Peterson, S. B. Bacterial competition: surviving and thriving in the microbial jungle. Nat. Rev. Microbiol. 8, 15–25 (2010)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Turnbaugh, P. J. et al. The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Sci. Transl. Med. 1, 6ra14 (2009)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  60. Rainey, P. B. & Travisano, M. Adaptive radiation in a heterogeneous environment. Nature 394, 69–72 (1998)

    Article  ADS  CAS  PubMed  Google Scholar 

  61. Barroso-Batista, J. et al. The first steps of adaptation of Escherichia coli to the gut are dominated by soft sweeps. PLoS Genet. 10, e1004182 (2014)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  62. Goodman, A. L. et al. Identifying genetic determinants needed to establish a human gut symbiont in its habitat. Cell Host Microbe 6, 279–289 (2009)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Schluter, J., Nadell, C. D., Bassler, B. L. & Foster, K. R. Adhesion as a weapon in microbial competition. ISME J. 9, 139–149 (2015)

    Article  CAS  PubMed  Google Scholar 

  64. Thompson, J. A., Oliveira, R. A., Djukovic, A., Ubeda, C. & Xavier, K. B. Manipulation of the quorum sensing signal AI-2 affects the antibiotic-treated gut microbiota. Cell Rep. 10, 1861–1871 (2015)

    Article  CAS  PubMed  Google Scholar 

  65. Waller, A. S. et al. Classification and quantification of bacteriophage taxa in human gut metagenomes. ISME J. 8, 1391–1402 (2014)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Niehus, R., Mitri, S., Fletcher, A. G. & Foster, K. R. Migration and horizontal gene transfer divide microbial genomes into multiple niches. Nat. Commun. 6, 8924 (2015)

    Article  ADS  CAS  PubMed  Google Scholar 

  67. McInerney, J. O., McNally, A. & O’Connell, M. J. Why prokaryotes have pangenomes. Nat. Microbiol. 2, 17040 (2017)

    Article  CAS  PubMed  Google Scholar 

  68. Ji, B. & Nielsen, J. From next-generation sequencing to systematic modeling of the gut microbiome. Front. Genet. 6, 219 (2015)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  69. Rakoff-Nahoum, S ., Coyne, M. J . & Comstock, L. E. An ecological network of polysaccharide utilization among human intestinal symbionts. Curr. Biol. 24, 40–49 (2014). Experimental evidence of complex ecological interactions between Bacteroides species of the human gut via polysaccharide utilization

    Article  CAS  PubMed  Google Scholar 

  70. Cuskin, F. et al. Human gut Bacteroidetes can utilize yeast mannan through a selfish mechanism. Nature 517, 165–169 (2015)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  71. Nadell, C. D., Foster, K. R. & Xavier, J. B. Emergence of spatial structure in cell groups and the evolution of cooperation. PLoS Comput. Biol. 6, e1000716 (2010)

    Article  ADS  PubMed  PubMed Central  CAS  Google Scholar 

  72. Schluter, J., Schoech, A. P., Foster, K. R. & Mitri, S. The evolution of quorum sensing as a mechanism to infer kinship. PLoS Comput. Biol. 12, e1004848 (2016)

    Article  ADS  PubMed  PubMed Central  CAS  Google Scholar 

  73. Mark Welch, J. L., Rossetti, B. J., Rieken, C. W., Dewhirst, F. E. & Borisy, G. G. Biogeography of a human oral microbiome at the micron scale. Proc. Natl Acad. Sci. USA 113, E791–E800 (2016). Striking evidence of the spatial structure of different bacterial species in the oral microbiome

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  74. Earle, K. A. et al. Quantitative imaging of gut microbiota spatial organization. Cell Host Microbe 18, 478–488 (2015)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Faith, J. J. et al. The long-term stability of the human gut microbiota. Science 341, 1237439 (2013)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  76. Dethlefsen, L. & Relman, D. A. Incomplete recovery and individualized responses of the human distal gut microbiota to repeated antibiotic perturbation. Proc. Natl Acad. Sci. USA 108, 4554–4561 (2011)

    Article  ADS  CAS  PubMed  Google Scholar 

  77. Weimer, P. J. Redundancy, resilience, and host specificity of the ruminal microbiota: implications for engineering improved ruminal fermentations. Front. Microbiol. 6, 296 (2015)

    Article  PubMed  PubMed Central  Google Scholar 

  78. Scheffer, M. & van Nes, E. H. Self-organized similarity, the evolutionary emergence of groups of similar species. Proc. Natl Acad. Sci. USA 103, 6230–6235 (2006)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  79. Nyholm, S. V. & McFall-Ngai, M. J. The winnowing: establishing the squid–vibrio symbiosis. Nat. Rev. Microbiol. 2, 632–642 (2004)

    Article  CAS  PubMed  Google Scholar 

  80. Schwartzman, J. A. & Ruby, E. G. A conserved chemical dialog of mutualism: lessons from squid and vibrio. Microbes Infect. 18, 1–10 (2016). A review of the remarkable squid and Vibrio fischeri mutualism that shows strong host control

    Article  PubMed  Google Scholar 

  81. Brown, S. P. Cooperation and conflict in host-manipulating parasites. Proc. R. Soc. B 266, 1899–1904 (1999)

    Article  PubMed Central  Google Scholar 

  82. Brownlie, J. C. et al. Evidence for metabolic provisioning by a common invertebrate endosymbiont, Wolbachia pipientis, during periods of nutritional stress. PLoS Pathog. 5, e1000368 (2009)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  83. Correa, C. C. & Ballard, J. Wolbachia associations with insects: winning or losing against a master manipulator. Front. Ecol. Evol. 3, 153 (2016)

    Article  Google Scholar 

  84. Andersen, S. B. et al. The life of a dead ant: the expression of an adaptive extended phenotype. Am. Nat. 174, 424–433 (2009)

    Article  ADS  PubMed  Google Scholar 

  85. Louca, S. et al. High taxonomic variability despite stable functional structure across microbial communities. Nat. Ecol. Evol. 1, 0015 (2016)

    Article  Google Scholar 

  86. Adlassnig, W., Peroutka, M. & Lendl, T. Traps of carnivorous pitcher plants as a habitat: composition of the fluid, biodiversity and mutualistic activities. Ann. Bot. (Lond.) 107, 181–194 (2010)

    Article  Google Scholar 

  87. Agler, M. T. et al. Microbial hub taxa link host and abiotic factors to plant microbiome variation. PLoS Biol. 14, e1002352 (2016)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  88. Moeller, A. H. et al. Cospeciation of gut microbiota with hominids. Science 353, 380–382 (2016)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  89. Thompson, J. N. Interaction and Coevolution (Chicago Univ. Press, 2014)

  90. Ayres, J. S. Cooperative microbial tolerance behaviors in host–microbiota mutualism. Cell 165, 1323–1331 (2016)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Kernbauer, E., Ding, Y. & Cadwell, K. An enteric virus can replace the beneficial function of commensal bacteria. Nature 516, 94–98 (2014). Challenges the notion that commensal bacteria provide specific benefits to the host by showing that some of these benefits are also provided by a virus

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  92. Rypien, K. L., Ward, J. R. & Azam, F. Antagonistic interactions among coral-associated bacteria. Environ. Microbiol. 12, 28–39 (2010)

    Article  CAS  PubMed  Google Scholar 

  93. Knoll, A. H. The multiple origins of complex multicellularity. Annu. Rev. Earth Planet. Sci. 39, 217–239 (2011)

    Article  ADS  CAS  Google Scholar 

  94. Williams, G. C. Adaptation and Natural Selection: A Critique of Some Current Evolutionary Thought (Princeton Univ. Press, 1966). Seminal text on evolutionary adaptation and the importance of understanding biological function

  95. Medzhitov, R. Toll-like receptors and innate immunity. Nat. Rev. Immunol. 1, 135–145 (2001)

    Article  CAS  PubMed  Google Scholar 

  96. Allen, R. C., Popat, R., Diggle, S. P. & Brown, S. P. Targeting virulence: can we make evolution-proof drugs? Nat. Rev. Microbiol. 12, 300–308 (2014)

    Article  CAS  PubMed  Google Scholar 

  97. King, K. C. et al. Rapid evolution of microbe-mediated protection against pathogens in a worm host. ISME J. 10, 1915–1924 (2016). Experimental evolution shows that colonization resistance can evolve as a byproduct of microbial competition

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Nölling, J. et al. Genome sequence and comparative analysis of the solvent-producing bacterium Clostridium acetobutylicum. J. Bacteriol. 183, 4823–4838 (2001)

    Article  PubMed  PubMed Central  Google Scholar 

  99. Smith, P. M. et al. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science 341, 569–573 (2013)

    Article  ADS  CAS  PubMed  Google Scholar 

  100. Mazmanian, S. K., Liu, C. H., Tzianabos, A. O. & Kasper, D. L. An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell 122, 107–118 (2005)

    Article  CAS  PubMed  Google Scholar 

  101. Wilson, D. S. A theory of group selection. Proc. Natl Acad. Sci. USA 72, 143–146 (1975)

    Article  ADS  CAS  PubMed  MATH  PubMed Central  Google Scholar 

  102. Wilson, D. S. Biological communities as functionally organized units. Ecology 78, 2018–2024 (1997)

    Article  Google Scholar 

  103. Williams, H. T. & Lenton, T. M. Environmental regulation in a network of simulated microbial ecosystems. Proc. Natl Acad. Sci. USA 105, 10432–10437 (2008)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

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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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Foster, K., Schluter, J., Coyte, K. et al. The evolution of the host microbiome as an ecosystem on a leash. Nature 548, 43–51 (2017). https://doi.org/10.1038/nature23292

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