Sociality in spiders is an evolutionary dead-end
Abstract
Sociality in spiders has evolved independently at least 23 times. However, their phylogenetic distribution suggests that all social species are of recent origin and evolutionarily short-lived. Here, we present genomic evidence for the evolutionary dead-end hypothesis in the three independent transitions to sociality observed 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 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 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.
Sociality in spiders is an evolutionary dead-end
Jilong Ma, Jesper Bechsgaard, Anne Aagaard, Palle Villesen, Trine Bilde, Mikkel Schierup
