Bacterial gut symbionts are tightly linked with the evolution of herbivory in ants

Ants are a dominant feature of terrestrial ecosystems, yet we know little about the forces that drive their evolution. Recent findings illustrate that their diets range from herbivorous to predaceous, with "herbivores" feeding primarily on exudates from plants and sap-feeding insects. Persistence on these nitrogen-poor food sources raises the question of how ants obtain sufficient nutrition. To investigate the potential role of symbiotic microbes, we have surveyed 283 species from 18 of the 21 ant subfamilies using molecular techniques. Our findings uncovered a wealth of bacteria from across the ants. Notable among the surveyed hosts were herbivorous "turtle ants" from the related genera <named-content content-type="genus-species">Cephalotes</named-content> and <named-content content-type="genus-species">Procryptocerus</named-content> (tribe Cephalotini). These commonly harbored bacteria from ant-specific clades within the <named-content content-type="genus-species">Burkholderiales</named-content>, <named-content content-type="genus-species">Pseudomonadales</named-content>, <named-content content-type="genus-species">Rhizobiales</named-content>, <named-content content-type="genus-species">Verrucomicrobiales</named-content>, and <named-content content-type="genus-species">Xanthomonadales</named-content>, and studies of lab-reared <named-content content-type="genus-species">Cephalotes varians</named-content> characterized these microbes as symbiotic residents of ant guts. Although most of these symbionts were confined to turtle ants, bacteria from an ant-specific clade of <named-content content-type="genus-species">Rhizobiales</named-content> were more broadly distributed. Statistical analyses revealed a strong relationship between herbivory and the prevalence of <named-content content-type="genus-species">Rhizobiales</named-content> gut symbionts within ant genera. Furthermore, a consideration of the ant phylogeny identified at least five independent origins of symbioses between herbivorous ants and related <named-content content-type="genus-species">Rhizobiales</named-content>. Combined with previous findings and the potential for symbiotic nitrogen fixation, our results strongly support the hypothesis that bacteria have facilitated convergent evolution of herbivory across the ants, further implicating symbiosis as a major force in ant evolution.