The Reproductive Microbiome: An Emerging Driver of Sexual Selection, Sexual Conflict, Mating Systems, and Reproductive Isolation
Authors: Melissah Rowe, Liisa Veerus, Pål Trosvik, Angus Buckling, Tommaso Pizzari
Journal: Trends in Ecology & Evolution (2020)

Although it is clear that the microbiome can have major influences on host biology, relatively little is known about the microbial communities in the reproductive systems of males and females.The reproductive microbiome can have significant effects on the reproductive function and fitness of males and females, although these effects are rarely considered from an ecological or evolutionary perspective.Recent research indicates that the reproductive microbiome can influence the outcomes of pre- and postcopulatory sexual selection, as well as generate conflict between the sexes.Thus, complex coevolutionary dynamics can emerge between the host mating system and the reproductive microbiome, to shape patterns of reproductive skew in the host, microbial diversity across individuals and species, and the ecology and evolution of reproductive microbes. Consequently, reproductive microbiomes also have strong potential to influence reproductive barriers between host populations. All multicellular organisms host microbial communities in and on their bodies, and these microbiomes can have major influences on host biology. Most research has focussed on the oral, skin, and gut microbiomes, whereas relatively little is known about the reproductive microbiome. Here, we review empirical evidence to show that reproductive microbiomes can have significant effects on the reproductive function and performance of males and females. We then discuss the likely repercussions of these effects for evolutionary processes related to sexual selection and sexual conflict, as well as mating systems and reproductive isolation. We argue that knowledge of the reproductive microbiome is fundamental to our understanding of the evolutionary ecology of reproductive strategies and sexual dynamics of host organisms. All multicellular organisms host microbial communities in and on their bodies, and these microbiomes can have major influences on host biology. Most research has focussed on the oral, skin, and gut microbiomes, whereas relatively little is known about the reproductive microbiome. Here, we review empirical evidence to show that reproductive microbiomes can have significant effects on the reproductive function and performance of males and females. We then discuss the likely repercussions of these effects for evolutionary processes related to sexual selection and sexual conflict, as well as mating systems and reproductive isolation. We argue that knowledge of the reproductive microbiome is fundamental to our understanding of the evolutionary ecology of reproductive strategies and sexual dynamics of host organisms. Animals and plants live and evolve in a world dominated by microbes, and host a diversity of microbial communities in and on their bodies. A recent explosion in research on host-associated microbial communities (i.e., microbiota and/or microbiomes, see Glossary) is revolutionising biology. While earlier research typically considered microorganisms from a pathological perspective, it is now widely accepted that the relationship between host and microbes spans a continuum, from detrimental to beneficial. Through their influence on host health, physiology, development, and behaviour [1Parfrey L.W. et al.Introduction: the host-associated microbiome: pattern, process and function.Mol. Ecol. 2018; 27: 1749-1765Crossref PubMed Scopus (5) Google Scholar,2Ezenwa V.O. et al.Animal behavior and the microbiome.Science. 2012; 338: 198-199Crossref PubMed Scopus (194) Google Scholar], microbiomes can be seen as an integral part of the host phenotype, and potentially also the host genome (e.g., the hologenome concept [3Rosenberg E. Zilber-Rosenberg I. Microbes drive evolution of animals and plants: the hologenome concept.mBio. 2016; 7: e01395Crossref PubMed Google Scholar], but see [4Moran N.A. Sloan D.B. The hologenome concept: helpful or hollow?.PLoS Biol. 2015; 13: e1002311Crossref PubMed Google Scholar]). While considerable attention has been paid to the role of oral, skin, and gut microbiomes in host ecology, evolution, and fitness, less is known about the reproductive microbiome (Box 1). This is surprising given longstanding knowledge of microbes in male and female reproductive systems (e.g., [5Rehewy M.S.E. et al.Aerobic and anaerobic bacterial flora in semen from fertile and infertile groups of men.Arch. Androl. 1979; 2: 263-268Crossref PubMed Scopus (0) Google Scholar]), most notably in the context of sexually transmitted infections (STIs) [6Lockhart A.B. et al.Sexually transmitted diseases in animals: ecological and evolutionary implications.Biol. Rev. 1996; 71: 415-471Crossref PubMed Google Scholar], and more recent DNA-sequencing studies demonstrating the presence of dynamic microbial communities in reproductive tissues [7Schoenmakers S. et al.The matter of the reproductive microbiome.Obstet. Med. 2019; 12: 107-115Crossref PubMed Scopus (1) Google Scholar], especially the vagina [8Ravel J. et al.Vaginal microbiome of reproductive-age women.Proc. Natl. Acad. Sci. U. S. A. 2011; 108: 4680-4687Crossref PubMed Scopus (1227) Google Scholar,9Chen C. et al.The microbiota continuum along the female reproductive tract and its relation to uterine-related diseases.Nat. Commun. 2017; 8: 875Crossref PubMed Scopus (0) Google Scholar]. Thus, the reproductive microbiome represents an outstanding challenge in the study of host-associated microbial communities.Box 1Defining the Reproductive MicrobiomeIn the broadest sense, the reproductive microbiome can be defined operationally as the microbiome, including bacteria, viruses and unicellular algae, protozoans and fungi, living in or on any structure, organ, fluid, or tissue of a host that typically makes contact with the gametes (or gamete analogues, e.g., pollen or gametophytes) or reproductive tract or organs of another individual through mating, spawning, or pollination. This captures the microbiomes associated with the reproductive system of a host, involved at any point in the reproductive process, from gamete production and release (e.g., ejaculation) and up to the point of fertilisation, including the microbiomes of male and female reproductive tracts, gametes, and reproductive fluids, as well as genitalia, intromittent organs and sperm transfer structures, (e.g., pedipalps of spiders, hectocotyli of cephalopods, aedeagi of insects, gonopods of millipedes, claspers of sharks and rays, gonopodium of Poeciliidae, and hemipenes of lizards and snakes), and spermatophores.This definition includes species that release gametes into the external environment, such as external fertilisers, wind- and vector-pollinated angiosperms, fern spores released in water, and animals that release sperm packages (e.g., spermatophores) on substrate for female uptake, as well as species where fertilisation is mediated by other organisms (e.g., pollination via animal vectors and externally fertilising fish that spawn within the gills of mussels, e.g., European bitterlings). In these cases, the reproductive microbiome reflects the microbiome associated with a set of released gametes, from which there is potential for members of the microbiome to colonise gametes of the opposite sex.While most research is currently focussed on a few host species, this broad definition enables us to develop arguments and hypotheses of broad generality. As we develop an understanding of the structural and functional diversity of reproductive microbiomes, more refined definitions may begin to emerge, with a narrower focus and more specialised to the biology of different systems. Such definitions might benefit from identifying the host and/or site of the microbiome (e.g., the human reproductive microbiome [7Schoenmakers S. et al.The matter of the reproductive microbiome.Obstet. Med. 2019; 12: 107-115Crossref PubMed Scopus (1) Google Scholar], the vaginal microbiome of primates [11Yildirim S. et al.Primate vaginal microbiomes exhibit species specificity without universal Lactobacillus dominance.ISME J. 2014; 8: 2431-2444Crossref PubMed Scopus (50) Google Scholar], or the microbiome of copulatory organs of spiders [108Spicer M.E. et al.Spiders, microbes and sex: bacterial exposure on copulatory organs alters mating behaviour in funnel-web spiders.Ethology. 2019; 92: 91-99Google Scholar]).An important challenge in the study of reproductive microbiomes is the limited knowledge that we have of these microbial communities. Currently, it is generally unclear how reproductive microbiomes are established or maintained, as well as the function they may have in relation to host mating dynamics and reproductive processes. Furthermore, due to the prevalence of microbiome mixing and chance events (see Box 2) it is unclear to which degree reproductive microbiomes represent native assemblages or more transient, random assemblages, and, in some instances, there is significant contribution from a range of sources, such as the external environment (e.g., microbiome of gametes released into the environment and external genitalia) and other body sites of the host. In many instances, the structure of reproductive microbiomes may be the result of both of random and deterministic processes, which may lead to spatiotemporal dynamics in these microbiomes. Consideration of these ecological processes may also lead to greater clarity in our understanding and definition of reproductive microbiomes in the future. In the broadest sense, the reproductive microbiome can be defined operationally as the microbiome, including bacteria, viruses and unicellular algae, protozoans and fungi, living in or on any structure, organ, fluid, or tissue of a host that typically makes contact with the gametes (or gamete analogues, e.g., pollen or gametophytes) or reproductive tract or organs of another individual through mating, spawning, or pollination. This captures the microbiomes associated with the reproductive system of a host, involved at any point in the reproductive process, from gamete production and release (e.g., ejaculation) and up to the point of fertilisation, including the microbiomes of male and female reproductive tracts, gametes, and reproductive fluids, as well as genitalia, intromittent organs and sperm transfer structures, (e.g., pedipalps of spiders, hectocotyli of cephalopods, aedeagi of insects, gonopods of millipedes, claspers of sharks and rays, gonopodium of Poeciliidae, and hemipenes of lizards and snakes), and spermatophores. This definition includes species that release gametes into the external environment, such as external fertilisers, wind- and vector-pollinated angiosperms, fern spores released in water, and animals that release sperm packages (e.g., spermatophores) on substrate for female uptake, as well as species where fertilisation is mediated by other organisms (e.g., pollination via animal vectors and externally fertilising fish that spawn within the gills of mussels, e.g., European bitterlings). In these cases, the reproductive microbiome reflects the microbiome associated with a set of released gametes, from which there is potential for members of the microbiome to colonise gametes of the opposite sex. While most research is currently focussed on a few host species, this broad definition enables us to develop arguments and hypotheses of broad generality. As we develop an understanding of the structural and functional diversity of reproductive microbiomes, more refined definitions may begin to emerge, with a narrower focus and more specialised to the biology of different systems. Such definitions might benefit from identifying the host and/or site of the microbiome (e.g., the human reproductive microbiome [7Schoenmakers S. et al.The matter of the reproductive microbiome.Obstet. Med. 2019; 12: 107-115Crossref PubMed Scopus (1) Google Scholar], the vaginal microbiome of primates [11Yildirim S. et al.Primate vaginal microbiomes exhibit species specificity without universal Lactobacillus dominance.ISME J. 2014; 8: 2431-2444Crossref PubMed Scopus (50) Google Scholar], or the microbiome of copulatory organs of spiders [108Spicer M.E. et al.Spiders, microbes and sex: bacterial exposure on copulatory organs alters mating behaviour in funnel-web spiders.Ethology. 2019; 92: 91-99Google Scholar]). An important challenge in the study of reproductive microbiomes is the limited knowledge that we have of these microbial communities. Currently, it is generally unclear how reproductive microbiomes are established or maintained, as well as the function they may have in relation to host mating dynamics and reproductive processes. Furthermore, due to the prevalence of microbiome mixing and chance events (see Box 2) it is unclear to which degree reproductive microbiomes represent native assemblages or more transient, random assemblages, and, in some instances, there is significant contribution from a range of sources, such as the external environment (e.g., microbiome of gametes released into the environment and external genitalia) and other body sites of the host. In many instances, the structure of reproductive microbiomes may be the result of both of random and deterministic processes, which may lead to spatiotemporal dynamics in these microbiomes. Consideration of these ecological processes may also lead to greater clarity in our understanding and definition of reproductive microbiomes in the future. Patterns of variation have been studied for some female reproductive microbiomes, due in part to an interest in understanding mother–child microbial transfer. In humans, microbiome composition varies across the female reproductive tract (e.g., vagina, cervix, uterus, fallopian tubes, and follicular fluid [9Chen C. et al.The microbiota continuum along the female reproductive tract and its relation to uterine-related diseases.Nat. Commun. 2017; 8: 875Crossref PubMed Scopus (0) Google Scholar,10Younes J.A. et al.Women and their microbes: the unexpected friendship.Trends Microbiol. 2018; 26: 16-32Abstract Full Text Full Text PDF PubMed Scopus (0) Google Scholar]). Intriguingly, the human vaginal microbiome is a relatively low-diversity environment, dominated by bacteria from the genus Lactobacillus [7Schoenmakers S. et al.The matter of the reproductive microbiome.Obstet. Med. 2019; 12: 107-115Crossref PubMed Scopus (1) Google Scholar,9Chen C. et al.The microbiota continuum along the female reproductive tract and its relation to uterine-related diseases.Nat. Commun. 2017; 8: 875Crossref PubMed Scopus (0) Google Scholar], whereas, in other mammals, lactobacilli rarely constitute >1% of the vaginal microbiome [11Yildirim S. et al.Primate vaginal microbiomes exhibit species specificity without universal Lactobacillus dominance.ISME J. 2014; 8: 2431-2444Crossref PubMed Scopus (50) Google Scholar, 12Swartz J.D. et al.Characterization of the vaginal microbiota of ewes and cows reveals a unique microbiota with low levels of lactobacilli and near-neutral pH.Front. Vet. Sci. 2014; 1: 19Crossref PubMed Google Scholar, 13Vrbanac A. et al.The murine vaginal microbiota and its perturbation by the human pathogen group B Streptococcus.BMC Microbiol. 2018; 18: 197Crossref PubMed Scopus (1) Google Scholar]. Several hypotheses have been proposed to explain the uniqueness of the human vaginal microbiome, including differences in reproductive physiology, disease risk, and diet [14Miller E.A. et al.Lactobacilli dominance and vaginal pH: why is the human vaginal microbiome unique?.Front. Microbiol. 2016; 7: 4-13Crossref PubMed Scopus (44) Google Scholar,15Stumpf R.M. et al.The primate vaginal microbiome: comparative context and implications for human health and disease.Am. J. Phys. Anthropol. 2013; 152: 119-134Crossref PubMed Google Scholar]. The female reproductive microbiome can be highly dynamic. For example, in primates, the vaginal microbiome changes with female age and life-history phase, menstruation, and pregnancy [7Schoenmakers S. et al.The matter of the reproductive microbiome.Obstet. Med. 2019; 12: 107-115Crossref PubMed Scopus (1) Google Scholar,15Stumpf R.M. et al.The primate vaginal microbiome: comparative context and implications for human health and disease.Am. J. Phys. Anthropol. 2013; 152: 119-134Crossref PubMed Google Scholar]. Intra- and interindividual variability has also been reported for the vaginal microbiome of mice, although factors influencing this variation are currently unclear (e.g., variation is not associated with oestrus cycling) [13Vrbanac A. et al.The murine vaginal microbiota and its perturbation by the human pathogen group B Streptococcus.BMC Microbiol. 2018; 18: 197Crossref PubMed Scopus (1) Google Scholar]. These findings are revolutionising our understanding of the female reproductive system and reproductive health, and have changed the perception of the female reproductive tract as a sterile environment. Less attention has been paid to the male reproductive microbiome. However, the ejaculate in a range of taxa is known to host microorganisms [16Poiani A. Complexity of seminal fluid: a review.Behav. Ecol. Sociobiol. 2006; 60: 289-310Crossref Scopus (288) Google Scholar]. High-throughput sequencing studies have shown that human ejaculates are typically characterised by low biomass microbial communities [7Schoenmakers S. et al.The matter of the reproductive microbiome.Obstet. Med. 2019; 12: 107-115Crossref PubMed Scopus (1) Google Scholar], thus, requiring special care during sample collection and processing to avoid erroneous results [17Koedooder R. et al.Identification and evaluation of the microbiome in the female and male reproductive tracts.Hum. Reprod. Update. 2019; 25: 298-325Crossref PubMed Scopus (4) Google Scholar]. In humans, the semen microbiome is more diverse (greater species richness) and exhibits greater species evenness than that of the vagina [7Schoenmakers S. et al.The matter of the reproductive microbiome.Obstet. Med. 2019; 12: 107-115Crossref PubMed Scopus (1) Google Scholar], although the two communities do share taxa. A reproductive microbiome has also been described from the seminal fluid of mice [18Javurek A.B. et al.Discovery of a novel seminal fluid microbiome and influence of estrogen receptor alpha genetic status.Sci. Rep. 2016; 6: 23027Crossref PubMed Scopus (25) Google Scholar] and the human penis [19Price L.B. et al.The effects of circumcision on the penis microbiome.PLoS One. 2010; 5: e8422Crossref PubMed Scopus (0) Google Scholar]. Here, we review evidence for the potential impact of reproductive microbiomes for host fertility and fitness, and discuss the functional implications of these impacts for sexual selection, sexual conflict, mating systems and strategies, and reproductive isolation. We also consider the microbial perspective (Box 2), because a full understanding of microbial community assembly, succession, and function requires consideration of the fitness interests of members of the microbiome. While reproductive microbiomes occur across the animal and plant kingdoms, and indeed are likely to have critical implications for both animal and plant hosts, most empirical work to date has focussed on dioecious, sexually reproducing animals with internal fertilisation. Therefore, we focus most of our discussion on these taxa, although the arguments proposed will have broad generality.Box 2Microbial Evolutionary Ecology of the Reproductive MicrobiomeA modified metacommunity framework is useful for understanding what shapes the composition of the microbiome [109Miller E.T. et al.Microbiomes as metacommunities: understanding host-associated microbes through metacommunity ecology.Trends Ecol. Evol. 2018; 33: 926-935Abstract Full Text Full Text PDF PubMed Scopus (0) Google Scholar]. Metacommunity dynamics assume that the composition of a local patch (i.e., a microbiome) is shaped by both local interactions and immigration from other microbiomes, as well as the external environment. Immigration from other microbiomes is likely to have a particularly important role in shaping reproductive microbiomes, given their inevitable large scale and, often frequent, mixing as a result of transmission during mating. Mixing will increase with increasing mating rates or increases in multiple mating by individuals, and is also greater in females than males. Coupled with the fluctuating selection pressures imposed both by changes in microbiome composition and within-host physiological status, the structure (and function) is likely to vary considerably through time [88Gajer P. et al.Temporal dynamics of the human vaginal microbiota.Sci. Transl. Med. 2012; 4: 132ra52Crossref PubMed Scopus (471) Google Scholar]. The propensity for extremely rapid evolution of microbes is also likely to have a major role in shaping these ecological dynamics, which in turn will drive evolutionary change [110Ellner S.P. et al.Does rapid evolution matter? Measuring the rate of contemporary evolution and its impacts on ecological dynamics.Ecol. Lett. 2011; 14: 603-614Crossref PubMed Scopus (155) Google Scholar].Arguably, one of the most important implications of a highly compositionally dynamic microbiome is that a 'holobiont or hologenome' perspective, which assumes that the host and (at least parts of) the microbiome are a unit of selection, is unlikely to be useful [4Moran N.A. Sloan D.B. The hologenome concept: helpful or hollow?.PLoS Biol. 2015; 13: e1002311Crossref PubMed Google Scholar]. The mixing of microbiomes between sexual partners, as well as potentially acquiring members of the microbiome from other external environments, means that most members of the microbiome are unlikely to be vertically cotransmitted with the host genome and, hence, will create potential evolutionary conflict between members of the microbiome and hosts, notably with respect to rates of sexual encounters.The mixing of microbiomes will also affect how the structure and function of the reproductive microbiome co-vary with host genotype, which can have a key role in, for example, the extent to which the microbiome might affect the evolution of host mate choice. From a purely ecological perspective, increased mixing of microbiomes will breakdown this covariance. However, mixing will have less predictable effects on the covariance between host genotype and microbial genotype. Microbes are likely to rapidly adapt to local host conditions (local adaptation; LA), increasing host–microbe genetic covariances. While high levels of migration will genetically homogenise populations, reducing LA, increased genetic variation resulting from immigration can also enhance LA by increasing the rate of adaptation [111Gandon S. et al.Local adaptation and gene-for-gene coevolution in a metapopulation model.Proc. R. Soc. B. 1997; 263: 1003-1009Google Scholar]. These effects of migration on LA will be reinforced by adaption to co-occurring community members, which can limit the invasion of foreign microbial communities [112Tikhonov M. Community-level cohesion without cooperation.eLife. 2016; 5: 86Crossref Scopus (22) Google Scholar]. If certain microbial taxa have key roles in determining microbiome function (although we do not yet know if this is the case), such microbe–host genetic covariances may have important implications.Microbial community composition and function can also be greatly affected by chance events, further reducing the specificity of microbiomes to their host genotypes [113Sprockett D. et al.Role of priority effects in the early-life assembly of the gut microbiota.Nat. Rev. Gastroenterol. Hepatol. 2018; 15: 197-205Crossref PubMed Scopus (38) Google Scholar]. Reproductive microbiomes, particularly vaginal, are regularly disturbed as a consequence of menstruation, enhancing the importance of priority effects [i.e., the dominance of early (re)colonising species] in shaping community assembly [114Fukami T. Historical contingency in community assembly: integrating niches, species pools, and priority effects.Annu. Rev. Ecol. Evol. Syst. 2015; 46: 1-23Crossref Scopus (338) Google Scholar]. Rapid (co)evolution of microbial populations can also lead to divergent community assemblies, as a result of the stochasticity of mutational events, and can potentially reshape entire microbial communities [115Gómez P. et al.Local adaptation of a bacterium is as important as its presence in structuring a natural microbial community.Nat. Commun. 2016; 7: 12453Crossref PubMed Scopus (21) Google Scholar].The phenotypic consequences of the reproductive microbiome on their host may mismatch host genotype even more than community composition. First, functional equivalence between taxa can weaken structure–function relationships [116Martiny J.B.H. et al.Microbiomes in light of traits: a phylogenetic perspective.Science. 2015; 350: aac9323Crossref PubMed Scopus (186) Google Scholar]. Second, microbiomes are complex ecosystems, often dominated by strongly competitive interactions [117Coyte K.Z. et al.The ecology of the microbiome: networks, competition, and stability.Science. 2015; 350: 663-666Crossref PubMed Scopus (354) Google Scholar]. These interactions may have a key role in shaping the phenotypic effects of the microbiome on its host. For example, interference and exploitation between microbes can be highly temporally varying traits as a result of coevolution, and can have an important impact on pathogenesis through the reductions in population and community size [118Inglis R.F. et al.Spite versus cheats: competition among social strategies shapes virulence in Pseudomonas aeruginosa.Evolution. 2012; 66: 3472-3484Crossref PubMed Scopus (13) Google Scholar]. Finally, some traits selected in response to competition [119O'Brien S. et al.Adaptation to public goods cheats in Pseudomonas aeruginosa.Proc. Biol. Sci. 2017; 284: 20171089Crossref PubMed Scopus (10) Google Scholar] can also directly affect hosts. A modified metacommunity framework is useful for understanding what shapes the composition of the microbiome [109Miller E.T. et al.Microbiomes as metacommunities: understanding host-associated microbes through metacommunity ecology.Trends Ecol. Evol. 2018; 33: 926-935Abstract Full Text Full Text PDF PubMed Scopus (0) Google Scholar]. Metacommunity dynamics assume that the composition of a local patch (i.e., a microbiome) is shaped by both local interactions and immigration from other microbiomes, as well as the external environment. Immigration from other microbiomes is likely to have a particularly important role in shaping reproductive microbiomes, given their inevitable large scale and, often frequent, mixing as a result of transmission during mating. Mixing will increase with increasing mating rates or increases in multiple mating by individuals, and is also greater in females than males. Coupled with the fluctuating selection pressures imposed both by changes in microbiome composition and within-host physiological status, the structure (and function) is likely to vary considerably through time [88Gajer P. et al.Temporal dynamics of the human vaginal microbiota.Sci. Transl. Med. 2012; 4: 132ra52Crossref PubMed Scopus (471) Google Scholar]. The propensity for extremely rapid evolution of microbes is also likely to have a major role in shaping these ecological dynamics, which in turn will drive evolutionary change [110Ellner S.P. et al.Does rapid evolution matter? Measuring the rate of contemporary evolution and its impacts on ecological dynamics.Ecol. Lett. 2011; 14: 603-614Crossref PubMed Scopus (155) Google Scholar]. Arguably, one of the most important implications of a highly compositionally dynamic microbiome is that a 'holobiont or hologenome' perspective, which assumes that the host and (at least parts of) the microbiome are a unit of selection, is unlikely to be useful [4Moran N.A. Sloan D.B. The hologenome concept: helpful or hollow?.PLoS Biol. 2015; 13: e1002311Crossref PubMed Google Scholar]. The mixing of microbiomes between sexual partners, as well as potentially acquiring members of the microbiome from other external environments, means that most members of the microbiome are unlikely to be vertically cotransmitted with the host genome and, hence, will create potential evolutionary conflict between members of the microbiome and hosts, notably with respect to rates of sexual encounters. The mixing of microbiomes will also affect how the structure and function of the reproductive microbiome co-vary with host genotype, which can have a key role in, for example, the extent to which the microbiome might affect the evolution of host mate choice. From a purely ecological perspective, increased mixing of microbiomes will breakdown this covariance. However, mixing will have less predictable effects on the covariance between host genotype and microbial genotype. Microbes are likely to rapidly adapt to local host conditions (local adaptation; LA), increasing host–microbe genetic covariances. While high levels of migration will genetically homogenise populations, reducing LA, increased genetic variation resulting from immigration can also enhance LA by increasing the rate of adaptation [111Gandon S. et al.Local adaptation and gene-for-gene coevolution in a metapopulation model.Proc. R. Soc. B. 1997; 263: 1003-1009Google Scholar]. These effects of migration on LA will be reinforced by adaption to co-occurring community members, which can limit the invasion of foreign microbial communities [112Tikhonov M. Community-level cohesion without cooperation.eLife. 2016; 5: 86Crossref Scopus (22) Google Scholar]. If certain microbial taxa have key roles in determining microbiome function (although we do not yet know if this is the case), such microbe–host genetic covariances may have important implications. Microbial community composition and function can also be greatly affected by chance events, further reducing the specificity of microbiomes to their host genotypes [113Sprockett D. et al.Role of priority effects in the early-life as