Convergent molecular evolution associated with repeated transitions to gregarious larval behaviour in Heliconiini

Abstract Collective behavior forms the basis for many antipredator strategies. Within Lepidoptera, larval gregariousness has evolved convergently across many phylogenetically disparate lineages. While the selection pressures shaping variation in larval social behaviors are well investigated, much less is known about the mechanisms that control social attraction and behavioral coordination. Similarly, little is known about how secondary selection pressures associated with social living shape genome evolution. Here, using genomic data for over 60 species from an adaptive radiation of Neotropical butterflies, the Heliconiini, in which gregarious behavior has evolved repeatedly, we explore the molecular basis of repeated convergent shifts toward gregarious larvae. We focus on three main areas of genomic evolution: differential selection on homologous genes, accelerated rates of evolution on noncoding regions of key genes, and differential gene expression in the brains of solitary and gregarious larvae. We identify strong signatures of convergent molecular evolution, on both coding and noncoding loci, in Heliconiini lineages, which evolved gregarious behavior. Molecular convergence is also detected at the transcriptomic level in larval brains, suggesting convergent shifts in gene regulation in neural tissue. Among loci showing strong signals of convergent evolution in gregarious lineages, we identify several strong candidates linked to neural activity, feeding behavior, and immune pathways. Our results suggest social living profoundly changes the selection pressures acting on multiple physiological, immunological, and behavioral traits.