The diversification of mealybugs was triggered by new symbiont acquisitions and followed by adaptive radiations on host plants

Abstract

Symbiotic microorganisms play a critical role in supplementing beneficial nutrients to herbivorous insects feeding on unbalanced diets. These microbial symbionts can both facilitate or constrain plant-feeding insects adaptations to certain host plants, depending on their gene content and metabolic potential. The diet breadth of herbivorous insects is considered an important evolutionary factor affecting genotypic and phenotypic changes associated with host shifts. Acquiring new symbionts can, therefore, drive changes in niche breadth and subsequent adaptive radiation(s). Mealybugs comprise one of the major groups of scale insects, most of which feed on diverse angiosperms. Different sub-lineages of mealybugs also house different lineages of bacteria and fungi as their obligate symbionts. Here, we use mealybugs as a model system to test the hypothesis that the evolution of herbivorous insects is driven by both obligate symbionts and host plants. Based on metagenome analyses of 28 host species as well as a literature survey, we identified Betaproteobacteria, Gammaproteobacteria, Flavobacteriia, and Ophiocordyceps fungi as obligate symbionts of the major clades of mealybugs. A time-calibrated phylogenetic tree of mealybugs allowed us to infer the ancestral obligate symbionts of the major mealybug clades. Our results indicate that the emergence of major mealybug lineages coincided with the acquisitions of new obligate endosymbionts. Subsequent radiations of mealybugs were inferred to have mostly resulted from the adaptive radiation through continuous host shifts on angiosperms. The contribution of microbial symbiosis to the diversification of herbivorous insects is thus likely limited by new symbiont origins or replacements, and insect adaptations play a larger role in further plant switches.