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

Abstract

With one of the highest number of parasite, eusocial and pollinator species among all insect orders, Hymenoptera features a great diversity of specific lifestyles. At the population genetic level, such life-history strategies are expected to decrease effective population size and efficiency of purifying selection. In this study, we tested this hypothesis by estimating the relative rate of non-synonymous substitution in 169 species to investigate the variation in natural selection efficiency throughout the hymenopteran tree of life. We found no effect of parasitism or body size, but show that relaxed selection is associated with eusociality, suggesting that the division of reproductive labour decreases effective population size in ants, bees and wasps. Unexpectedly, the effect of eusociality is marginal compared to 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. This widespread pattern suggests specific constraints in pollinating bees potentially linked to limited resource and high parental investment. The particularly high load of deleterious mutations we report in the genome of these crucial ecosystem engineer species also raises new concerns about their ongoing population decline.