Phylosymbiosis: Relationships and Functional Effects of Microbial Communities across Host Evolutionary History

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.

Author Summary

Studies on the assembly and function of host-microbiota symbioses are inherently complicated by the diverse effects of diet, age, sex, host genetics, and endosymbionts. Central to unraveling one effect from the other is an experimental framework that reduces confounders. Using common rearing conditions across four animal groups (deer mice, flies, mosquitoes, and wasps) that span recent host speciation events to more distantly related host genera, this study tests whether microbial community assembly is generally random with respect to host relatedness or "phylosymbiotic," in which the phylogeny of the host group is congruent with ecological relationships of their microbial communities. Across all four animal groups and one external dataset of great apes, we apply several statistics for analyzing congruencies and demonstrate phylosymbiosis to varying degrees in each group. Moreover, consistent with selection on host–microbiota interactions driving phylosymbiosis, transplanting interspecific microbial communities in mice significantly decreased their ability to digest food. Similarly, wasps that received transplants of microbial communities from different wasp species had lower survival than those given their own microbiota. Overall, this experimental and statistical framework shows how microbial community assembly and functionality across related species can be linked to animal evolution, health, and survival.