The genomic consequences and persistence of sociality in spiders

Abstract

In cooperatively breeding social animals, a few individuals account for all reproduction. In some taxa, sociality is accompanied by a transition from outcrossing to inbreeding, in concert, these traits act to reduce effective population size, potentially rendering transitions to sociality evolutionarily dead-ends. We addressed this hypothesis in a comparative genomic study in spiders, where sociality has evolved independently at least 23 times, but social species are recent and evolutionarily short-lived. We present genomic evidence for the evolutionary dead-end hypothesis in three independent transitions to sociality in the spider genus Stegodyphus. We sequenced, assembled and annotated high-quality, chromosome-level reference genomes from three pairs of closely related social and subsocial Stegodyphus species. Genome sizes range from 2.65 Gb to 3.32 Gb with high synteny, and we identify 10,065 single-copy orthologous genes. We timed the divergence between the social and subsocial species pairs to be from 1.3 to 1.8 million years. Social evolution in spiders involves a shift from outcrossing to inbreeding and from equal to female-biased sex ratio, causing severe reductions in effective population size and decreased efficacy of selection. Based on analyses of purifying selection, we determined whether transitions to sociality co-occurred with divergence. We show that transitions to sociality only had full effect on purifying selection at 119 kya (95CI: 71 kya -169 kya), 260 kya (95CI: 231 ky - 289 kya) and 279 kya (95CI: 230 kya - 332 kya) respectively, and follow remarkably similar convergent trajectories of progressive loss of diversity and shifts to an increasingly female-biased sex ratio. This almost deterministic genomic response to sociality may explain why social spider species do not persist. What causes species extinction is not clear, but could be either selfish meiotic drive that eliminates the production of males, or an inability to retain genome integrity in the face of extremely reduced efficacy of selection.