Repeated Evolution of Sociality is Associated with Reduced Mutation Rates in Spiders

Germline mutation rates influence the pace of molecular evolution, yet the roles of selection and life history in shaping their evolution remain to be determined. Comparative systems with replicated evolutionary transitions provide a unique opportunity to determine how changes in life history influence germline mutation rates. In the spider genus Stegodyphus, permanent sociality evolved independently three times within the past million years and is associated with obligate inbreeding, female-biased sex ratios, reduced fecundity, and sharply reduced effective population sizes. We sequenced 202 parent-offspring trios from 34 full-sibling families across three social and four closely related subsocial species and analysed quality-filtered trios in a phylogenetic comparative framework. Each independent transition to sociality was associated with an approximately 2-fold reduction in the de novo mutation rate in the germline. Phylogenetic analyses of synonymous branch lengths suggest that the mutation rates declined in parallel with the transitions to sociality. These rapid reductions in mutation rates in social lineages with small effective population sizes run counter to the drift-barrier hypothesis, which predicts that reduced selection efficacy would lead to higher mutation rates. We find no evidence that reduced mutation rates in the social species was favoured by selection for improving DNA repair efficiency, since there is no upregulation of DNA repair pathway genes in the ovaries of the social species. On the contrary, the mutation rate is reduced across mutational classes and in somatic tissue in social species compared with their subsocial counterparts. These patterns suggest that the reduction in mutation rate in social spiders is a consequence of convergent life history changes, including reduced body size and production of fewer, larger eggs. Our results highlight that the evolution of sociality, which entails major life history changes, can rapidly reshape fundamental evolutionary parameters, such as the germline mutation rate.