Relaxation of purifying selection suggests low effective population size in eusocial Hymenoptera and pollinating bees

Eusociality is a rare life history strategy that evolved repeatedly in Hymenoptera. At the population genetics level, inbreeding and low effective population size have been suggested as both evolutionary causes and consequences of social life. In this study, we tested these hypotheses by estimating the relative rate of non-synonymous substitution in 169 species to investigate the variation in natural selection efficiency and effective population size throughout the Hymenoptera tree of life. We show that relaxed selection is strongly associated with eusociality. This suggests that the division of reproductive labour decreases effective population size in ants, bees and wasps. Interestingly, we also report a striking and widespread relaxation of selection in both social and non social bees, which indicates that these keystone pollinator species generally feature low effective population sizes. We suggest that a particularly high inbreeding rate in bees might increase the benefits of kin selection, which would explain why most independent origins of eusociality in the tree of life occurred in this taxon. The particularly high load of deleterious mutations we report in the genome of these crucial ecosystem engineer species suggest new concerns about their ongoing population decline.