Worker Reproduction and Caste Polymorphism Impact Genome Evolution and Social Genes Across the Ants

Eusocial insects are characterized by several traits, including reproductive division of labor and caste polymorphisms, which likely modulate genome evolution. Concomitantly, evolution may act on specific genes and pathways underlying these novel, sociality-associated phenotypes. Reproductive division of labor should increase the magnitude of genetic drift and reduce the efficacy of selection by reducing effective population size. Caste polymorphism has been associated with relaxed selection and may facilitate directional selection on caste-specific genes. Here, we use comparative analyses of 22 ant genomes to test how reproductive division of labor and worker polymorphism influence positive selection and selection intensity across the genome. Our results demonstrate that worker reproductive capacity is associated with a reduction in the degree of relaxed selection but is not associated with any significant change to positive selection. We find decreases in positive selection in species with polymorphic workers, but no increase in the degree of relaxed selection. Finally, we explore evolutionary patterns in specific candidate genes associated with our focal traits in eusocial insects. Two oocyte patterning genes previously implicated in worker sterility evolve under intensified selection in species with reproductive workers. Behavioral caste genes generally experience relaxed selection associated with worker polymorphism, whereas vestigial and spalt, both associated with soldier development in Pheidole ants, experience intensified selection in worker polymorphic species. These findings expand our understanding of the genetic mechanisms underlying elaborations of sociality. The impacts of reproductive division of labor and caste polymorphisms on specific genes illuminate those genes' roles in generating complex eusocial phenotypes.