SRA

Evolutionary adaptations for the exploitation of nutritionally challenging or toxic host plants represent a major driving force behind the diversification of phytophagous insects. Although symbiotic bacteria are known to play essential nutritional roles for insects, examples of adaptive radiations into novel ecological niches following the acquisition of specific symbionts remain scarce. Here we characterized the microbiota across bugs of the family Pyrrhocoridae and investigated whether the acquisition of vitamin-supplementing symbionts enabled the hosts’ adaptive radiation on the nutritionally imbalanced and chemically well-defended seeds of Malvales plants as a food source. Our results indicate that vitamin-provisioning Actinobacteria (Coriobacterium and Gordonibacter), as well as Firmicutes (Clostridium) and Proteobacteria (Klebsiella) are widespread across Pyrrhocoridae, but absent from the sister family Largidae and other outgroup taxa. Despite the consistent association with a specific microbiota, the Pyrrhocoridae phylogeny is neither congruent with a dendrogram based on the hosts’ microbial community profiles nor phylogenies of individual symbiont strains, indicating frequent horizontal exchange of symbiotic partners. Phylogenetic dating analyses based on the fossil record reveal an origin of the Pyrrhocoridae core microbiota in the late Cretaceous (81.2-86.5 mya), following the transition from crypt-associated beta-proteobacterial symbionts to an anaerobic community localized in the M3 region of the mid-gut. The change in symbiotic syndromes (i.e. symbiont identity and localization) and the acquisition of the pyrrhocorid core microbiota coincided with the evolution of their preferred host plants (Malvales), suggesting that the symbionts enabled their hosts to successfully exploit this imbalanced nutritional resource and subsequently diversify in a competition-poor ecological niche.