Convergent evolution associated with the loss of developmental diapause may promote extended lifespan in bees

Abstract

Diapause has long been proposed to play a significant role in the evolution of eusociality in Hymenoptera. Recent studies have shown that shifts in the diapause stage precede social evolution in wasps and bees, however, the genomic basis remains unknown. Given the overlap in molecular pathways that regulate diapause and lifespan, we hypothesized that the evolutionary loss of developmental diapause may lead to extended lifespan among adults, which is a prerequisite for the evolution of eusociality. To test this, we compared 27 bee genomes with or without prepupal diapause. Our results point to several potential mechanisms for lifespan extension in species lacking prepupal diapause, including the loss of the growth hormone PTTH and its receptor TORSO, along with convergent selection in genes known to regulates lifespan in animals. Specifically, we observed purifying selection of pro-longevity genes and relaxed selection of anti-longevity genes within the IIS/TOR pathway in species that have lost prepupal diapause. Changes in selection pressures on this pathway may lead to the evolution of new phenotypes, such as lifespan extension and altered responses to nutritional signals, that are crucial for social evolution. SignificanceDiapause has long been proposed to play a significant role in the evolution of eusociality in Hymenoptera. Recent studies have shown that the loss of diapause during the prepupal stage precedes social evolution in wasps and bees. However, the genomic mechanisms underlying this phenomenon remain unknown. Through comparative genomics, we showed that the convergent loss of prepupal diapause is associated with mechanisms that may promote lifespan extension, a prerequisite for social evolution. These mechanisms include genes losses and signals of selection on genes related to aging.