Rethinking the epigenetic foundations of social behavior evolution in insects

Gene body DNA methylation is an evolutionarily conserved, stable yet reversible modification of DNA, where cytosines in CpG contexts are covalently methylated (5-methyl-cytosine) by DNA methyltransferase (DNMT) enzymes. The discovery of a functional gene body DNA methylation system in honey bees (Apis mellifera L.) with high homology to the human machinery has positioned social insects, including wasps, ants, and bees, as tractable models for epigenetic research. Their advanced societies consist of multiple phenotypes with distinct morphologies, physiologies, and behaviors, all developed from the same genome. Here we examine seminal studies on DNA methylation in social Hymenoptera, focusing on three recent advances: (i) gene body DNA methylation has minimal, if any, effect on transcription; (ii) methylomes are faithfully inherited across generations and somatic tissues; and (iii) DNMT1 is essential for the germline but dispensable for somatic development. As a mechanistic complement to Hamilton's inclusive fitness theory, we propose that colony-specific gene body DNA methylation patterns may facilitate (but not determine) the multiple independent transitions to eusociality in Hymenoptera. With the framework of a 'DNA methylation-mediated Genetic Recombination Hypothesis', we suggest that DNMT1-maintained gene body DNA methylation accelerates genome evolution toward social complexity in eusocial species. On the other hand, DNMT3, likely operating downstream of the sex-determination pathways, promotes altruism in sterile workers in the presence of the queen, possibly through DNA methylation-independent mechanisms.