Phylosymbiosis Impacts Adaptive Traits in Nasonia Wasps

Phylosymbiosis is an ecoevolutionary hypothesis and emerging pattern in animal-microbiota studies whereby the host phylogenetic relationships parallel the community relationships of the host-associated microbiota. A central prediction of phylosymbiosis is that closely related hosts exhibit a lower microbiota beta diversity than distantly related hosts. While phylosymbiosis has emerged as a widespread trend in a field often challenged to find trends across systems, two critical and understudied questions are whether or not phylosymbiosis is consequential to host biology and if adaptive evolutionary forces underpin the pattern. Here, using germfree rearing in the phylosymbiosis model Nasonia, we demonstrate that early life exposure to heat-inactivated microbiota from more distantly related species poses more severe developmental and survival costs than microbiota from closely related or the same species. This study advances a functional understanding of the consequences and potential selective pressures underpinning phylosymbiosis. ABSTRACT Phylosymbiosis is defined as microbial community relationships that recapitulate the phylogeny of hosts. As evidence for phylosymbiosis rapidly accumulates in different vertebrate and invertebrate holobionts, a central question is what evolutionary forces cause this pattern. We use intra- and interspecific gut microbiota transplants to test for evidence of selective pressures that contribute to phylosymbiosis. We leverage three closely related species of the parasitoid wasp model Nasonia that recently diverged between 0.4 and 1 million years ago: N. vitripennis, N. giraulti, and N. longicornis. Upon exposure of germfree larvae to heat-inactivated microbiota from intra- or interspecific larvae, we measure larval growth, pupation rate, and adult reproductive capacity. We report three key findings: (i) larval growth significantly slows when hosts receive an interspecific versus intraspecific gut microbiota, (ii) marked decreases in pupation and resulting adult survival occur from interspecific gut microbiota exposure, and (iii) adult reproductive capacities including male fertility and longevity are unaffected by early life exposure to an interspecific microbiota. Overall, these findings reveal developmental and survival costs to Nasonia upon larval exposures to interspecific microbiota and provide evidence that selective pressures on phenotypes produced by host-microbiota interactions may underpin phylosymbiosis. IMPORTANCE Phylosymbiosis is an ecoevolutionary hypothesis and emerging pattern in animal-microbiota studies whereby the host phylogenetic relationships parallel the community relationships of the host-associated microbiota. A central prediction of phylosymbiosis is that closely related hosts exhibit a lower microbiota beta diversity than distantly related hosts. While phylosymbiosis has emerged as a widespread trend in a field often challenged to find trends across systems, two critical and understudied questions are whether or not phylosymbiosis is consequential to host biology and if adaptive evolutionary forces underpin the pattern. Here, using germfree rearing in the phylosymbiosis model Nasonia, we demonstrate that early life exposure to heat-inactivated microbiota from more distantly related species poses more severe developmental and survival costs than microbiota from closely related or the same species. This study advances a functional understanding of the consequences and potential selective pressures underpinning phylosymbiosis.