1.Bercik, P. et al. The intestinal microbiota affect central levels of brain-derived neurotropic factor and behavior in mice. Gastroenterology 141, 599–609 (2011).CAS 
 PubMed 
 Google Scholar 
 2.Johnson, K. V.-A. & Foster, K. R. Why does the microbiome affect behaviour? Nat. Rev. Microbiol. 16, 647–655 (2018).CAS 
 PubMed 
 Google Scholar 
 3.Sherwin, E., Bordenstein, S. R., Quinn, J. L., Dinan, T. G. & Cryan, J. F. Microbiota and the social brain. Science 366, eaar2016 (2019).CAS 
 PubMed 
 Google Scholar 
 4.Charbonneau, M. R. et al. A microbial perspective of human developmental biology. Nature 535, 48–55 (2016).CAS 
 PubMed 
 PubMed Central 
 Google Scholar 
 5.Blanton, L. V. et al. Gut bacteria that prevent growth impairments transmitted by microbiota from malnourished children. Science 351, aad3311 (2016).PubMed 
 Google Scholar 
 6.Matsuoka, K. & Kanai, T. The gut microbiota and inflammatory bowel disease. Semin. Immunopathol. 37, 47–55 (2015).CAS 
 PubMed 
 Google Scholar 
 7.Niu, B., Paulson, J. N., Zheng, X. & Kolter, R. Simplified and representative bacterial community of maize roots. Proc. Natl Acad. Sci. USA 114, E2450–E2459 (2017).CAS 
 PubMed 
 PubMed Central 
 Google Scholar 
 8.Berg, M. & Koskella, B. Nutrient- and dose-dependent microbiome-mediated protection against a plant pathogen. Curr. Biol. 28, 2487–2492 (2018).CAS 
 PubMed 
 Google Scholar 
 9.Wei, Z. et al. Trophic network architecture of root-associated bacterial communities determines pathogen invasion and plant health. Nat. Commun. 6, 8413 (2015).10.Keebaugh, E. S., Yamada, R., Obadia, B., Ludington, W. B. & William, W. J. Microbial quantity impacts Drosophila nutrition, development, and lifespan. iScience 4, 247–259 (2018).CAS 
 PubMed 
 PubMed Central 
 Google Scholar 
 11.Camarinha-Silva, A. et al. Host genome influence on gut microbial composition and microbial prediction of complex traits in pigs. Genetics 206, 1637–1644 (2017).CAS 
 PubMed 
 PubMed Central 
 Google Scholar 
 12.Difford, G. F. et al. Host genetics and the rumen microbiome jointly associate with methane emissions in dairy cows. PLoS Genet. 14, e1007580 (2018).PubMed 
 PubMed Central 
 Google Scholar 
 13.Moran, N. A. & Sloan, D. B. The hologenome concept: helpful or hollow? PLoS Biol. 13, e1002311 (2015).PubMed 
 PubMed Central 
 Google Scholar 
 14.Henry, L. P., Bruijning, M., Forsberg, S. K. G. & Ayroles, J. F. The microbiome extends host evolutionary potential. Nat. Commun. 12, 5141 (2021).15.Foster, K. R., Schluter, J., Coyte, K. Z. & Rakoff-Nahoum, S. The evolution of the host microbiome as an ecosystem on a leash. Nature 548, 43–51 (2017).CAS 
 PubMed 
 PubMed Central 
 Google Scholar 
 16.Baumann, P. Biology of bacteriocyte-associated endosymbionts of plant sap-sucking insects. Annu. Rev. Microbiol. 59, 155–189 (2005).CAS 
 PubMed 
 Google Scholar 
 17.Douglas, A. E. Nutritional interactions in insect–microbial symbioses: aphids and their symbiotic bacteria Buchnera. Annu. Rev. Entomol. 43, 17–37 (1998).CAS 
 PubMed 
 Google Scholar 
 18.Roughgarden, J., Gilbert, S. F., Rosenberg, E., Zilber-Rosenberg, I. & Lloyd, E. A. Holobionts as units of selection and a model of their population dynamics and evolution. Biol. Theory 13, 44–65 (2018).
 Google Scholar 
 19.Fukatsu, T. & Hosokawa, T. Capsule-transmitted gut symbiotic bacterium of the Japanese common plataspid stinkbug, Megacopta punctatissima. Appl. Environ. Microbiol. 68, 389–396 (2002).CAS 
 PubMed 
 PubMed Central 
 Google Scholar 
 20.Kaiwa, N. et al. Symbiont-supplemented maternal investment underpinning host’s ecological adaptation. Curr. Biol. 24, 2465–2470 (2014).CAS 
 PubMed 
 Google Scholar 
 21.Jahnes, B. C., Herrmann, M. & Sabree, Z. L. Conspecific coprophagy stimulates normal development in a germ-free model invertebrate. PeerJ 7, e6914 (2019).PubMed 
 PubMed Central 
 Google Scholar 
 22.Estes, A. M. et al. Brood ball-mediated transmission of microbiome members in the dung beetle, Onthophagus taurus (Coleoptera: Scarabaeidae). PLoS ONE 8, e79061 (2013).CAS 
 PubMed 
 PubMed Central 
 Google Scholar 
 23.van Vliet, S. & Doebeli, M. The role of multilevel selection in host microbiome evolution. Proc. Natl Acad. Sci. USA 116, 20591–20597 (2019).PubMed 
 PubMed Central 
 Google Scholar 
 24.Zeng, Q., Wu, S., Sukumaran, J. & Rodrigo, A. Models of microbiome evolution incorporating host and microbial selection. Microbiome 5, 127 (2017).25.Björk, J. R., Diez-Vives, C., Astudillo-Garcia, C., Archie, E. A. & Montoya, J. M. Vertical transmission of sponge microbiota is inconsistent and unfaithful. Nat. Ecol. Evol. 3, 1172–1183 (2019).PubMed 
 PubMed Central 
 Google Scholar 
 26.Douglas, A. E. & Werren, J. H. Holes in the hologenome: why host–microbe symbioses are not holobionts. mBio 7, e02099-15 (2016).PubMed 
 PubMed Central 
 Google Scholar 
 27.Hammer, T. J. & Moran, N. A. Links between metamorphosis and symbiosis in holometabolous insects. Phil. Trans. R. Soc. B 374, 20190068 (2019).CAS 
 PubMed 
 PubMed Central 
 Google Scholar 
 28.Metcalf, C. J. E., Henry, L. P., Rebolleda-Gomez, M. & Koskella, B. Why evolve reliance on the microbiome for timing of ontogeny?. mBio 10, e01496-19 (2019).PubMed 
 PubMed Central 
 Google Scholar 
 29.Bruijning, M., Metcalf, C. J. E., Jongejans, E. & Ayroles, J. F. The evolution of variance control. Trends Ecol. Evol. 35, 22–23 (2020).PubMed 
 Google Scholar 
 30.Bull, J. J. Evolution of phenotypic variance. Evolution 41, 303–315 (1987).CAS 
 PubMed 
 Google Scholar 
 31.Philippi, T. & Seger, J. Hedging one’s evolutionary bets, revisited. Trends Ecol. Evol. 4, 41–44 (1989).CAS 
 PubMed 
 Google Scholar 
 32.Vasseur, D. A. & Yodzis, P. The color of environmental noise. Ecology 85, 1146–1152 (2004).
 Google Scholar 
 33.Halley, J. M. Ecology, evolution and 1f-noise. Trends Ecol. Evol. 11, 33–37 (1996).CAS 
 PubMed 
 Google Scholar 
 34.Botero, C. A., Weissing, F. J., Wright, J. & Rubenstein, D. R. Evolutionary tipping points in the capacity to adapt to environmental change. Proc. Natl Acad. Sci. USA 112, 184–189 (2015).CAS 
 PubMed 
 Google Scholar 
 35.Burns, A. R. et al. Contribution of neutral processes to the assembly of gut microbial communities in the zebrafish over host development. ISME J. 10, 655–664 (2016).CAS 
 PubMed 
 Google Scholar 
 36.Kolodny, O. et al. Coordinated change at the colony level in fruit bat fur microbiomes through time. Nat. Ecol. Evol. 3, 116–124 (2019).PubMed 
 Google Scholar 
 37.Sieber, M. et al. Neutrality in the metaorganism. PLoS Biol. 17, e3000298 (2019).PubMed 
 PubMed Central 
 Google Scholar 
 38.Burns, A. R. et al. Interhost dispersal alters microbiome assembly and can overwhelm host innate immunity in an experimental zebrafish model. Proc. Natl Acad. Sci. USA 114, 11181–11186 (2017).CAS 
 PubMed 
 PubMed Central 
 Google Scholar 
 39.Moeller, A. H., Suzuki, T. A., Phifer-Rixey, M. & Nachman, M. W. Transmission modes of the mammalian gut microbiota. Science 362, 453–457 (2018).CAS 
 PubMed 
 Google Scholar 
 40.Zapién-Campos, R., Sieber, M. & Traulsen, A. Stochastic colonization of hosts with a finite lifespan can drive individual host microbes out of equilibrium. PLoS Comput. Biol. 16, e1008392 (2020).PubMed 
 PubMed Central 
 Google Scholar 
 41.De Vries, E. J., Jacobs, G., Sabelis, M. W., Menken, S. B. J. & Breeuwer, J. A. J. Diet-dependent effects of gut bacteria on their insect host: the symbiosis of Erwinia sp. and western flower thrips. Proc. R. Soc. Lond. B 271, 2171–2178 (2004).
 Google Scholar 
 42.Johnson, N. C., Graham, J. H. & Smith, F. A. Functioning of mycorrhizal associations along the mutualism–parasitism continuum. N. Phytol. 135, 575–585 (1997).
 Google Scholar 
 43.Cheney, K. L. & Côté, I. M. Mutualism or parasitism? The variable outcome of cleaning symbioses. Biol. Lett. 1, 162–165 (2005).PubMed 
 PubMed Central 
 Google Scholar 
 44.Russell, J. A. & Moran, N. A. Costs and benefits of symbiont infection in aphids: variation among symbionts and across temperatures. Proc. R. Soc. B 273, 603–610 (2006).PubMed 
 Google Scholar 
 45.Oliver, K. M., Degnan, P. H., Burke, G. R. & Moran, N. A. Facultative symbionts in aphids and the horizontal transfer of ecologically important traits. Annu. Rev. Entomol. 55, 247–266 (2010).CAS 
 PubMed 
 Google Scholar 
 46.Oliver, K. M., Russell, J. A., Moran, N. A. & Hunter, M. S. Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc. Natl Acad. Sci. USA 100, 1803–1807 (2003).CAS 
 PubMed 
 PubMed Central 
 Google Scholar 
 47.Oliver, K. M., Campos, J., Moran, N. A. & Hunter, M. S. Population dynamics of defensive symbionts in aphids. Proc. R. Soc. B 275, 293–299 (2008).PubMed 
 Google Scholar 
 48.Ives, A. R. et al. Self-perpetuating ecological–evolutionary dynamics in an agricultural host–parasite system. Nat. Ecol. Evol. 4, 702–711 (2020).PubMed 
 Google Scholar 
 49.Chen, D.-Q., Montllor, C. B. & Purcell, A. H. Fitness effects of two facultative endosymbiotic bacteria on the pea aphid, Acyrthosiphon pisum, and the blue alfalfa aphid, A. kondoi. Entomol. Exp. Appl. 95, 315–323 (2000).
 Google Scholar 
 50.Montllor, C. B., Maxmen, A. & Purcell, A. H. Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress. Ecol. Entomol. 27, 189–195 (2002).
 Google Scholar 
 51.Kikuchi, Y. et al. Symbiont-mediated insecticide resistance. Proc. Natl Acad. Sci. USA 109, 8618–8622 (2012).CAS 
 PubMed 
 PubMed Central 
 Google Scholar 
 52.Kikuchi, Y. & Yumoto, I. Efficient colonization of the bean bug Riptortus pedestris by an environmentally transmitted Burkholderia symbiont. Appl. Environ. Microbiol. 79, 2088–2091 (2013).CAS 
 PubMed 
 PubMed Central 
 Google Scholar 
 53.Gould, A. L. et al. Microbiome interactions shape host fitness. Proc. Natl Acad. Sci. USA 115, E11951–E11960 (2018).CAS 
 PubMed 
 PubMed Central 
 Google Scholar 
 54.Ellner, S. P. & Rees, M. Integral projection models for species with complex demography. Am. Nat. 167, 410–428 (2006).PubMed 
 Google Scholar 
 55.Caswell, H. Matrix Population Models: Construction, Analysis and Interpretation (Sinauer Associates, 2001).56.Asnicar, F. et al. Studying vertical microbiome transmission from mothers to infants by strain-level metagenomic profiling. mSystems 2, e00164-16 (2017).PubMed 
 PubMed Central 
 Google Scholar 
 57.Yassour, M. et al. Strain-level analysis of mother-to-child bacterial transmission during the first few months of life. Cell Host Microbe 24, 146–154 (2018).CAS 
 PubMed 
 PubMed Central 
 Google Scholar 
 58.Ferretti, P. et al. Mother-to-infant microbial transmission from different body sites shapes the developing infant gut microbiome. Cell Host Microbe 24, 133–145 (2018).CAS 
 PubMed 
 PubMed Central 
 Google Scholar 
 59.Nyholm, S. V. & McFall-Ngai, M. The winnowing: establishing the squid-Vibrio symbiosis. Nat. Rev. Microbiol. 2, 632–642 (2004).CAS 
 PubMed 
 Google Scholar 
 60.Kikuchi, Y., Hosokawa, T. & Fukatsu, T. Insect–microbe mutualism without vertical transmission: a stinkbug acquires a beneficial gut symbiont from the environment every generation. Appl. Environ. Microbiol. 73, 4308–4316 (2007).CAS 
 PubMed 
 PubMed Central 
 Google Scholar 
 61.Ibáñez, F., Tonelli, M. L., Muñoz, V., Figueredo, M. S. & Fabra, A. in Endophytes: Biology and Biotechnology (ed. Maheshwari, D.) 25–40 (Springer, 2017).62.Werren, J. H., Baldo, L. & Clark, M. E. Wolbachia: master manipulators of invertebrate biology. Nat. Rev. Microbiol. 6, 741–751 (2008).CAS 
 PubMed 
 Google Scholar 
 63.Teixeira, L., Ferreira, Á. & Ashburner, M. The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Biol. 6, 2753–2763 (2008).CAS 
 Google Scholar 
 64.Chrostek, E. et al. Wolbachia variants induce differential protection to viruses in Drosophila melanogaster: a phenotypic and phylogenomic analysis. PLoS Genet. 9, e1003896 (2013).PubMed 
 PubMed Central 
 Google Scholar 
 65.Chrostek, E. & Teixeira, L. Mutualism breakdown by amplification of Wolbachia genes. PLoS Biol. 13, e1002065 (2015).PubMed 
 PubMed Central 
 Google Scholar 
 66.Ravel, C., Michalakis, Y. & Charmet, G. The effect of imperfect transmission on the frequency of mutualistic seed-borne endophytes in natural populations of grasses. Oikos 80, 18–24 (1997).
 Google Scholar 
 67.Buskirk, S. W., Rokes, A. B. & Lang, G. I. Adaptive evolution of nontransitive fitness in yeast. eLife 9, e62238 (2020).CAS 
 PubMed 
 PubMed Central 
 Google Scholar 
 68.Clune, J. et al. Natural selection fails to optimize mutation rates for long-term adaptation on rugged fitness landscapes. PLoS Comput. Biol. 4, e1000187 (2008).PubMed 
 PubMed Central 
 Google Scholar 
 69.King, O. D. & Masel, J. The evolution of bet-hedging adaptations to rare scenarios. Theor. Popul. Biol. 72, 560–575 (2007).PubMed 
 PubMed Central 
 Google Scholar 
 70.Liu, X.-D., Lei, H.-X. & Chen, F.-F. Infection pattern and negative effects of a facultative endosymbiont on its insect host are environment-dependent. Sci. Rep. 9, 4013 (2019).71.Oyserman, B. O. et al. Extracting the GEMs: genotype, environment, and microbiome interactions shaping host phenotypes. Front. Microbiol. 11, 3444 (2021).
 Google Scholar 
 72.Rock, D. I. et al. Context-dependent vertical transmission shapes strong endosymbiont community structure in the pea aphid, Acyrthosiphon pisum. Mol. Ecol. 27, 2039–2056 (2018).PubMed 
 Google Scholar 
 73.Osaka, R., Nomura, M., Watada, M. & Kageyama, D. Negative effects of low temperatures on the vertical transmission and infection density of a Spiroplasma endosymbiont in Drosophila hydei. Curr. Microbiol. 57, 335–339 (2008).CAS 
 PubMed 
 Google Scholar 
 74.Gundel, P. E. et al. Imperfect vertical transmission of the endophyte Neotyphodium in exotic grasses in grasslands of the Flooding Pampa. Microb. Ecol. 57, 740 (2009).PubMed 
 Google Scholar 
 75.Li, L. & Ma, Z. S. Testing the neutral theory of biodiversity with human microbiome datasets. Sci. Rep. 6, 31448 (2016).CAS 
 PubMed 
 PubMed Central 
 Google Scholar 
 76.Foster, K. R. & Bell, T. Competition, not cooperation, dominates interactions among culturable microbial species. Curr. Biol. 22, 1845–1850 (2012).CAS 
 PubMed 
 Google Scholar 
 77.Sprockett, D., Fukami, T. & Relman, D. A. Role of priority effects in the early-life assembly of the gut microbiota. Nat. Rev. Gastroenterol. Hepatol. 15, 197–205 (2018).PubMed 
 PubMed Central 
 Google Scholar 
 78.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).PubMed 
 PubMed Central 
 Google Scholar 
 79.Scheuring, I. & Yu, D. W. How to assemble a beneficial microbiome in three easy steps. Ecol. Lett. 15, 1300–1307 (2012).PubMed 
 PubMed Central 
 Google Scholar 
 80.Roughgarden, J. Holobiont evolution: Mathematical model with vertical vs. horizontal microbiome transmission. Phil. Theory Pract. Biol. 12, 002 (2020).81.Theis, K. R. et al. Getting the hologenome concept right: an eco-evolutionary framework for hosts and their microbiomes. mSystems 1, e00028-16 (2016).PubMed 
 PubMed Central 
 Google Scholar 
 82.Sloan, W. T. et al. Quantifying the roles of immigration and chance in shaping prokaryote community structure. Environ. Microbiol. 8, 732–740 (2006).PubMed 
 Google Scholar 
 83.Gillespie, J. Polymorphism in random environments. Theor. Popul. Biol. 4, 193–195 (1973).
 Google Scholar 
 84.Bruijning, M. Code for: Natural selection for imprecise vertical transmission in host-microbiota systems. Zenodo https://doi.org/10.5281/zenodo.5534317 (2021).85.Sauer, C., Dudaczek, D., Hölldobler, B. & Gross, R. Tissue localization of the endosymbiotic bacterium “Candidatus Blochmannia floridanus” in adults and larvae of the carpenter ant Camponotus floridanus. Appl. Environ. Microbiol. 68, 4187–4193 (2002).CAS 
 PubMed 
 PubMed Central 
 Google Scholar 
 86.Koga, R., Meng, X.-Y., Tsuchida, T. & Fukatsu, T. Cellular mechanism for selective vertical transmission of an obligate insect symbiont at the bacteriocyte–embryo interface. Proc. Natl Acad. Sci. USA 109, E1230–E1237 (2012).CAS 
 PubMed 
 PubMed Central 
 Google Scholar 
 87.Brentassi, M. E. et al. Bacteriomes of the corn leafhopper, Dalbulus maidis (DeLong & Wolcott, 1923) (Insecta, Hemiptera, Cicadellidae: Deltocephalinae) harbor Sulcia symbiont: molecular characterization, ultrastructure, and transovarial transmission. Protoplasma 254, 1421–1429 (2017).CAS 
 PubMed 
 Google Scholar 
 88.Picazo, D. R. et al. Horizontally transmitted symbiont populations in deep-sea mussels are genetically isolated. ISME J. 13, 2954–2968 (2019).
 Google Scholar 
 89.Gilbert, J. A. et al. Current understanding of the human microbiome. Nat. Med. 24, 392–400 (2018).CAS 
 PubMed 
 PubMed Central 
 Google Scholar 
 90.Korpela, K. et al. Selective maternal seeding and environment shape the human gut microbiome. Genome Res. 28, 561–568 (2018).CAS 
 PubMed 
 PubMed Central 
 Google Scholar 
 91.Walters, W. A. et al. Large-scale replicated field study of maize rhizosphere identifies heritable microbes. Proc. Natl Acad. Sci. USA 115, 7368–7373 (2018).PubMed 
 PubMed Central 
 Google Scholar 
 92.Douglas, A. E. Simple animal models for microbiome research. Nat. Rev. Microbiol. 17, 764–775 (2019).CAS 
 PubMed 
 Google Scholar 
 93.Sommer, F. et al. The gut microbiota modulates energy metabolism in the hibernating brown bear Ursus arctos. Cell Rep. 14, 1655–1661 (2016).CAS 
 PubMed 
 Google Scholar 
 94.David, L. A. et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature 505, 559–563 (2014).CAS 
 PubMed 
 Google Scholar  More