Comparative Transcriptomics of Convergent Evolution: Different Genes but Conserved Pathways Underlie Caste Phenotypes across Lineages of Eusocial Insects

An area of great interest in evolutionary genomics is whether convergently evolved traits are the result of convergent molecular mechanisms. The presence of queen and worker castes in insect societies is a spectacular example of convergent evolution and phenotypic plasticity. Multiple insect lineages have evolved environmentally induced alternative castes. Given multiple origins of eusociality in Hymenoptera (bees, ants, and wasps), it has been proposed that insect castes evolved from common genetic toolkits consisting of deeply conserved genes. Here, we combine data from previously published studies on fire ants and honey bees with new data for Polistes metricus paper wasps to assess the toolkit idea by presenting the first comparative transcriptome-wide analysis of caste determination among three major hymenopteran social lineages. Overall, we found few shared caste differentially expressed transcripts across the three social lineages. However, there is substantially more overlap at the levels of pathways and biological functions. Thus, there are shared elements but not on the level of specific genes. Instead, the toolkit appears to be relatively loose, that is, different lineages show convergent molecular evolution involving similar metabolic pathways and molecular functions but not the exact same genes. Additionally, our paper wasp data do not support a complementary hypothesis that novel taxonomically restricted genes are related to caste differences.