Abstract
Phylosymbiosis was recently proposed to describe the eco-evolutionary pattern, whereby the ecological relatedness of host-associated microbial communities parallels the phylogeny of related host species. Here, we test the prevalence of phylosymbiosis and its functional significance under highly controlled conditions by characterizing the microbiota of 24 animal species from four different groups (Peromyscus deer mice, Drosophila flies, mosquitoes, and Nasonia wasps), and we reevaluate the phylosymbiotic relationships of seven species of wild hominids. We demonstrate three key findings. First, intraspecific microbiota variation is consistently less than interspecific microbiota variation, and microbiota-based models predict host species origin with high accuracy across the dataset. Interestingly, the age of host clade divergence positively associates with the degree of microbial community distinguishability between species within the host clades, spanning recent host speciation events (~1 million y ago) to more distantly related host genera (~108 million y ago). Second, topological congruence analyses of each group's complete phylogeny and microbiota dendrogram reveal significant degrees of phylosymbiosis, irrespective of host clade age or taxonomy. Third, consistent with selection on host–microbiota interactions driving phylosymbiosis, there are survival and performance reductions when interspecific microbiota transplants are conducted between closely related and divergent host species pairs. Overall, these findings indicate that the composition and functional effects of an animal's microbial community can be closely allied with host evolution, even across wide-ranging timescales and diverse animal systems reared under controlled conditions.
Highlights
A large body of literature has documented genetic and environmental influences on the composition of host-associated microbial communities [1,2,3,4,5,6,7,8,9,10]
Are host–microbiota associations stochastically assembled, or might there be deterministic assembly mechanisms that predict these associations? How rapidly do microbiota differences form between closely related host species, and are interspecific microbiota differences prone to decay over evolutionary time? Can hostdriven assembly of the microbiota be isolated from confounding variables such as diet, age, sex, and endosymbionts? If there are microbiota differences between species, are they functional in an evolutionarily informed manner, such that mismatches between host and interspecific microbiota lead to reductions in fitness or performance, when interspecific microbiota transplants are conducted between older host species pairs?
Phylosymbiosis predicts that host clades will harbor distinguishable microbial communities and that more closely related host clades will exhibit more similar microbial communities
Summary
A large body of literature has documented genetic and environmental influences on the composition of host-associated microbial communities [1,2,3,4,5,6,7,8,9,10]. If host-associated microbial communities assemble stochastically through environmental acquisition with no host-specific influence, microbiota compositions across related host species will not differ from expectations based on random community assemblies and dispersal limitations. In a common environment, microbiota will form independent of host species (Fig 1A), and any interspecific differences in microbiota composition would be arbitrary. If microbial communities are distinguishable, hosts with greater genetic divergence may exhibit more distinguishable microbiota In this case, there will be congruence between the host phylogeny and microbiota dendrogram (Fig 1D). Phylosymbiosis refers to an eco-evolutionary pattern in which evolutionary changes in the host associate with ecological changes in the microbiota
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