Genomic signatures of recent convergent transitions to social life in spiders

Abstract

The transition from solitary to social life is a major phenotypic innovation, but its genetic underpinnings are largely unknown. To identify genomic changes associated with this transition, we compare the genomes of 22 spider species representing eight recent and independent origins of sociality. Hundreds of genes tend to experience shifts in selection during the repeated transition to social life. These genes are associated with several key functions, such as neurogenesis, behavior, and metabolism, and include genes that previously have been implicated in animal social behavior and human behavioral disorders. In addition, social species have elevated genome-wide rates of molecular evolution associated with relaxed selection caused by reduced effective population size. Altogether, our study provides unprecedented insights into the genomic signatures of social evolution and the specific genetic changes that repeatedly underpin the evolution of sociality. Our study also highlights the heretofore unappreciated potential of transcriptomics using ethanol-preserved specimens for comparative genomics and phylotranscriptomics.

Advances in the reconstruction of the spider tree of life: A roadmap for spider systematics and comparative studies

“…Sociality has been estimated to have evolved independently about 18 times in spiders (Agnarsson et al., 2006) in various families such as Oxyopidae and Theridiidae. Recent studies have found convergent expressions of certain gene families in the social spider species (Tong et al., 2022). A stable placement of Eresidae is thus important to understand the evolution of social behaviour in spiders.…”

Convergent genomics and Arctic adaptation of ruminants

“…This phenomenon of convergent phenotypic evolution serves as a powerful framework to uncover the genetic underpinnings of adaptations to specific environments, as these phenotypic convergences commonly emerge due to parallel selective pressures. With the increasing accessibility of genomic datasets of diverse species, a growing body of recent studies on convergent phenotypic evolution has unveiled remarkable genomic similarities across distinct lineages [3][4][5][6][7][8][9]. Convergent phenotypic evolution is hypothesized to be associated with various genetic mechanisms of genomic convergences.…”

“…For decades, studies on genomic convergences have primarily concentrated on the evolutionary dynamics of proteincoding genes [1][2][3][4][7][8][9]. By contrast, recent comparative genomic studies have begun to focus on the molecular evolution of non-coding regions across the genomes of diverse species, Types of genomic convergence.…”

“…The shift in rate of molecular evolution involves focal foreground taxa experiencing increasing d N /d S ratios compared to background taxa, indicating acceleration. Conversely, the decrease in d N /d S ratios in foreground taxa relative to background taxa suggests deceleration (figure 1 b ) [3,10]; the observation of concerted shifts in the intensity of natural selection—either relaxation or intensification (figure 1 b ). The degree to which shifts in the distributions of d N /d S ratio across individual genes or whole genomes can be caused by relaxation (weakening of both purifying selection and positive selection, towards neutrality) versus intensification (strengthening of both purifying selection and positive selection, away from neutrality) (figure 1 b ) [3]; and the identification of common signatures of positive selection which is the d N /d S ratios of specific genes or loci in focal taxa high than 1 [4,8].…”

“…Conversely, the decrease in d N /d S ratios in foreground taxa relative to background taxa suggests deceleration (figure 1 b ) [3,10]; the observation of concerted shifts in the intensity of natural selection—either relaxation or intensification (figure 1 b ). The degree to which shifts in the distributions of d N /d S ratio across individual genes or whole genomes can be caused by relaxation (weakening of both purifying selection and positive selection, towards neutrality) versus intensification (strengthening of both purifying selection and positive selection, away from neutrality) (figure 1 b ) [3]; and the identification of common signatures of positive selection which is the d N /d S ratios of specific genes or loci in focal taxa high than 1 [4,8]. Furthermore, previous studies have detected substantial convergences in gene family dynamics, notably gene loss or gain, among species exhibiting similar phenotypic traits (figure 1 c ) [5,9].…”