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

Abstract

AbstractSociality 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.Significance StatementThe transition from solitary to social life is a major transition in evolution that repeatedly occurred, but the genetic underpinnings are largely unknown. To identify genomic changes associated with sociality, we compared the genomes of 24 spider species, representing seven recent and independent origins of sociality. We identified hundreds of genes and many functional classes of genes that tended to experience shifts in molecular evolution, including genes that have previously been implicated in animal social behavior and human behavioral disorders. Our study shows that while the precise genetic details vary, the repeated evolution of sociality in spiders predictably leaves genome-wide signatures and involves sets of genes with conserved functions that may play general roles in the evolution of social behavior.