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Genome-wide, genic, and site-specific changes associated with the convergent evolution of sociality in spiders

By Chao Tong, Leticia Aviles, Linda Rayor, Alexander S. Mikheyev, Timothy A. Linksvayer

Posted 28 Jan 2021
bioRxiv DOI: 10.1101/2021.01.27.428473

Sociality is a striking phenotypic innovation that independently evolved dozens of times across animals. Sociogenomic approaches have begun to elucidate the molecular underpinnings of social life in social insects and vertebrates, but the degree to which the convergent evolution of sociality involves convergent molecular evolution remains controversial and largely unknown. Spiders are a powerful system for identifying the genomic causes and consequences of social life because sociality is estimated to have independently evolved 15 times, and each origin likely occurred recently, within the past few million years. To determine if there are statistically supported genomic signatures of protein-coding sequence evolution associated with the convergent evolution of sociality in spiders, we compared the genomes or transcriptomes of 24 spider species that vary in social organization and represent at least seven independent origins of sociality. We identified hundreds of genes that experienced shifts in patterns of molecular evolution during the convergent evolution of sociality, and these genes were enriched for several annotated functions, including neural function, neurogenesis, and behavior, as well as immune function, growth, and metabolism. We also found evidence that directional selection for specific substitutions repeatedly occurred in social species for several genes, in particular the calcium channel gene TPC1. Finally, supporting previous results, we found elevated genome-wide rates of molecular evolution in social species, resulting mainly from relaxation of selection. Altogether, we identify genome-wide, genic, and site-specific changes that repeatedly occurred during the evolution of sociality in spiders.

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