Convergent Evolution of Sociality Causes Reduction of Mutation Rates in Spiders

Germline mutations play a crucial role in determining the rate of molecular evolution. In the spider genus Stegodyphus, sociality has independently evolved three times within the past million years, each transition accompanied by major life history shifts, including obligate inbreeding, highly female biased sex ratios, reduced fecundity, and drastically lowered effective population sizes. We conducted whole genome sequencing of 202 parent-offspring trios from 34 families across three social and four subsocial species to estimate mutation rates in a phylogenetic comparative framework. Strikingly, each independent transition to sociality is associated with an approximately 50% reduction in germline mutation rate. This reduction has persisted over evolutionary timescales and suggests that mutation rates can decline rapidly, even in lineages with small effective population sizes, departing from predictions of the drift barrier hypothesis, which posits that mutation rates should increase under stronger genetic drift. We propose that the observed decline arises from life history mediated changes in germline dynamics such as slower development and fewer germline cell divisions, rather than direct selection on DNA repair efficiency. Our results highlight how social evolution can reshape fundamental genomic parameters and caution against assuming static mutation rates in evolutionary inference, underscoring the importance of ecological and developmental context in interpreting mutation rate variation.