Ants are among the most successful organisms on Earth. It has been suggested that forming symbioses with nutrient-supplementing microbes may have contributed to their success, by allowing ants to invade otherwise inaccessible niches. However, it is unclear whether ants have evolved symbioses repeatedly to overcome the same nutrient limitations. Here, we address this question by comparing the independently evolved symbioses in Camponotus, Plagiolepis, Formica and Cardiocondyla ants. Our analysis reveals the only metabolic function consistently retained in all of the symbiont genomes is the capacity to synthesise tyrosine. We also show that in certain multi-queen lineages that have co-diversified with their symbiont for millions of years, only a fraction of queens carry the symbiont, suggesting ants differ in their colony-level reliance on symbiont-derived resources. Our results imply that symbioses can arise to solve common problems, but hosts may differ in their dependence on symbionts, highlighting the evolutionary forces influencing the persistence of long-term endosymbiotic mutualisms.

Ants are among the most successful organisms on earth. It has been suggested that forming symbioses with nutrient-supplementing microbes may have contributed to their success, by allowing ants to invade otherwise inaccessible niches. However, it is unclear whether ants have repeatedly evolved symbioses to overcome the same nutrient limitations. Here, we address this question by comparing the independently evolved symbioses in Camponotus, Cardiocondyla, Formica and Plagiolepis ants. Our analysis reveals the only metabolic function consistently retained in all of the symbiont genomes is the capacity to synthesise tyrosine, which is essential for insect cuticles. We also reveal that in certain multi-queen lineages, only a fraction of queens carry the symbiont, suggesting ants differ in their colony-level reliance on symbiont-derived nutrients. Our results suggest symbioses can arise to solve common problems, but hosts may differ in their dependence on symbionts, highlighting the evolutionary forces influencing the persistence of long-term endosymbiotic mutualisms.

IntroductionInsects share intimate relationships with microbes that play important roles in their biology. Yet our understanding of how host-bound microbial communities assemble and perpetuate over evolutionary time is limited. Ants host a wide range of microbes with diverse functions and are an emerging model for studying the evolution of insect microbiomes. Here, we ask whether phylogenetically related ant species have formed distinct and stable microbiomes.MethodsTo answer this question, we investigated the microbial communities associated with queens of 14 Formica species from five clades, using deep coverage 16S rRNA amplicon sequencing.ResultsWe reveal that Formica species and clades harbor highly defined microbial communities that are dominated by four bacteria genera: Wolbachia, Lactobacillus, Liliensternia, and Spiroplasma. Our analysis reveals that the composition of Formica microbiomes mirrors the phylogeny of the host, i.e., phylosymbiosis, in that related hosts harbor more similar microbial communities. In addition, we find there are significant correlations between microbe co-occurrences.DiscussionOur results demonstrate Formica ants carry microbial communities that recapitulate the phylogeny of their hosts. Our data suggests that the co-occurrence of different bacteria genera may at least in part be due to synergistic and antagonistic interactions between microbes. Additional factors potentially contributing to the phylosymbiotic signal are discussed, including host phylogenetic relatedness, host-microbe genetic compatibility, modes of transmission, and similarities in host ecologies (e.g., diets). Overall, our results support the growing body of evidence that microbial community composition closely depends on the phylogeny of their hosts, despite bacteria having diverse modes of transmission and localization within the host.