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.

Terrestriality and bacterial transfer: a comparative study of gut microbiomes in sympatric Malagasy mammals

“…Rather than entire gut microbial communities, specific bacterial lineages may indeed recapitulate the evolutionary relationships among lemur species [9,22]. Further, lemur species may have diverged too recently [18] or our evolutionary model may be too simplistic to capture a strong signal of host phylogeny in the microbial community data.…”

“…With the exception of the lemur clade, the microbiomes of sympatric Malagasy mammal populations illustrate "phylosymbiosis," an ecoevolutionary pattern in which the evolutionary diversification of hosts correlates with ecological changes in their microbiota [18,74]. Congruence between host and microbial phylogenies can arise without the coevolution of entire microbial communities from a last common ancestor or cospeciation events [9,18].…”

“…Congruence between host and microbial phylogenies can arise without the coevolution of entire microbial communities from a last common ancestor or cospeciation events [9,18]. Thus, phylosymbiosis does not presuppose that all resident phylotypes in microbiomes are stable or vertically transmitted between generations [9,18]. For example, closely related hosts with comparable behavioral traits may acquire similar bacteria from their environment or directly from other hosts [9,75].…”

“…For example, closely related hosts with comparable behavioral traits may acquire similar bacteria from their environment or directly from other hosts [9,75]. In mammals, phylosymbiosis has been observed in large-scale comparative studies [9], among closely related species in controlled environments [18], and in wild populations of bats [16] and apes [8,76,77].…”

“…Several studies of zoo animals reared on artificial diets have claimed that diet and shared environment have greater impacts on gut microbiome composition than endogenous factors [10][11][12][13][14]. Other studies have focused on closely related mammal species and generally found that host species and their gut microbes exhibit concordant relationships [8,[15][16][17][18], with the gut microbial communities of different host species forming distinct clusters [18][19][20]. Within single host species, some studies of humans and other primates have suggested that social contact patterns are the primary predictor of gut microbiome composition [21][22][23][24][25], whereas others have found that host genetics exerts a strong influence [26,27].…”