Convergent selection on hormone signaling shaped social evolution in bees

Life’s dramatic innovations, from the emergence of self-replicating molecules to highly-integrated societies, often involve increases in biological complexity. Halictid bees have repeatedly gained and lost eusociality, a transition from individual to group reproduction. We developed powerful new comparative genomic resources for this group and identified complementary signatures of convergent selection associated with the emergence and breakdown of eusociality. We find that factors associated with the origins or maintenance of eusociality are also associated with its loss, indicating that there may be trade-offs, constraints, or costs associated with these genomic changes. We identify a subset of genes that experienced positive selection when eusociality arose and relaxed selection when eusociality was secondarily lost. Loci exhibiting these complementary signatures include two proteins that bind and transport juvenile hormone (JH) – a key regulator of insect development and reproduction. Both of these genes are differentially expressed between queens and workers in halictids, and brain single-cell RNA-sequencing reveals that one of these genes is specifically expressed in a cell cluster that co-expresses biomarkers of glial cells that make up the insect blood-brain-barrier. Taken together, our results help to explain how the evolution of a major transition was shaped by novel linkages between social behaviors, endocrine signaling, and brain physiology that have repeatedly evolved alongside eusociality in bees.