Natural selection during the recurrent evolution of a major social trait
A major question in evolutionary biology is understanding how complex novel phenotypes evolve. The 20,000 species of ants provide a unique framework to understand which genes are involved in social evolution and which tradeoffs underpin changes in social organization. Ants are characterized by a remarkable division of labor whereby individuals from specialized castes reproduce (queens, males) while others (workers) build and defend the nest, rear brood and forage for food. The ancestral social organization which evolved ~140 million years ago included a single queen and her highly related offspring. However, there have been at least 24 convergent evolutionary transitions from this ancestral social form to a derived form of social organization with multiple reproductive queens per colony. Importantly, differences in queen number are associated with major life history differences including dispersal strategy, intracolony relatedness, pathogen load, territoriality, intra- and inter-species competitiveness and ecological niche. These cases offer comparisons which can be used to identify potential genetic switches between different social systems. Our proposal will build extensively on the massive natural replication these large numbers of convergent occurrences provide. Are any genes or pathways consistently under different selection pressure after a species has transitioned to exclusively multiple-queen colonies? Does the derived form of social organization have additional effects on genome evolution such as reducing the efficacy of selection? We will address such questions using a strong phylogenomic framework encompassing 40 species and 15 convergent transitions. Our results will have major implications on our understanding of the mechanisms and costs involved in the evolution of this complex social phenotype.