Evolution of sociality in spiders leads to depleted genomic diversity at both population and species levels

Abstract

Across several animal taxa, the evolution of sociality involves a suite of characteristics, a "social syndrome," that includes cooperative breeding, reproductive skew, primary female-biased sex ratio, and the transition from outcrossing to inbreeding mating system, factors that are expected to reduce effective population size (Ne). This social syndrome may be favoured by short-term benefits but come with long-term costs, because the reduction in Ne amplifies loss of genetic diversity by genetic drift, ultimately restricting the potential of populations to respond to environmental change. To investigate the consequences of this social life form on genetic diversity, we used a comparative RAD-sequencing approach to estimate genomewide diversity in spider species that differ in level of sociality, reproductive skew and mating system. We analysed multiple populations of three independent sister-species pairs of social inbreeding and subsocial outcrossing Stegodyphus spiders, and a subsocial outgroup. Heterozygosity and within-population diversity were sixfold to 10-fold lower in social compared to subsocial species, and demographic modelling revealed a tenfold reduction in Ne of social populations. Species-wide genetic diversity depends on population divergence and the viability of genetic lineages. Population genomic patterns were consistent with high lineage turnover, which homogenizes the genetic structure that builds up between inbreeding populations, ultimately depleting genetic diversity at the species level. Indeed, species-wide genetic diversity of social species was 5-8 times lower than that of subsocial species. The repeated evolution of species with this social syndrome is associated with severe loss of genomewide diversity, likely to limit their evolutionary potential.

Ecological generalism facilitates the evolution of sociality in snapping shrimps

“…; Settepani et al . ). It is possible that eusociality is more common and more stable in snapping shrimps relative to the eusocial insects because of the intense competition that shrimps experience over host sponges.…”

Double-digest RAD-sequencing: do wet and dry protocol parameters impact biological results?

“…To estimate the influence of the m and M values on RAD tag fragment recovery, we determined the number of reconstructed fragments, their mean coverage and the proportion of polymorphic fragments for each value of M and m tested. We also evaluated the impact of these parameters on population genetics results by performing, for all m and M values, some of the most commonly used analyses using ddRADseq data (Capblancq et al, 2015; Kjeldsen et al, 2016; Black et al, 2017; Nunziata et al, 2017; Settepani et al, 2017; Elleouet & Aitken, 2018; Sherpa, Rioux, Pougnet-Lagarde, et al, 2018), i.e. mean individual heterozygosity, F ST among populations (estimated with the adegenet R package (Jombart, 2008)), Principal Component Analysis (PCA, using the adegenet R package (Jombart, 2008)), genetic structure with sNMF (using the LEA R package (Frichot & François, 2015)) and evolutionary history reconstruction using Approximate Bayesian Computation (performed with the diyABC program (Cornuet et al, 2014)).…”

“…Among these, double-digest RADseq, or ddRADseq (Peterson et al, 2012), is highly customizable as regards the final number of loci, depending on the choice of enzymes and range of fragment size selected. The ddRADseq approach has been applied with success to many purposes including population genetic studies (Kjeldsen et al, 2016; Black, Seears, Hollenbeck, & Samollow, 2017; Sherpa, Rioux, Goindin, et al, 2018), phylogenetic reconstructions (DaCosta & Sorenson, 2016; Vargas, Ortiz, & Simpson, 2017; Boubli et al, 2018; Lee et al, 2018; Sherpa, Rioux, Pougnet-Lagarde, & Després, 2018), demographic inferences (Capblancq, Després, Rioux, & Mavárez, 2015; Nunziata, Lance, Scott, Lemmon, & Weisrock, 2017; Settepani et al, 2017; Elleouet & Aitken, 2018) and landscape genetic analyses (Saenz-Agudelo et al, 2015; Johnson, Gaddis, Cairns, Konganti, & Krutovsky, 2017). Despite the recognized advantages of the ddRADseq technique, several limitations and weaknesses arose in the literature (Davey et al, 2013; K. R. Andrews et al, 2016; Lowry et al, 2017).…”

Comparative genomics identifies putative signatures of sociality in spiders

“…Relaxed purifying selection is expected to be especially common in species with low effective population size (N e ), and social species such as social spiders are expected to experience low N e as a result of reproductive skew, female-biased sex ratios, and inbreeding (Romiguier et al 2014;Galtier et al 2018;Settepani et al 2016). Indeed, previous studies in social spiders (Settepani et al 2016;Bechsgaard et al 2019;Settepani et al 2017Settepani et al , 2014 and also social insects have found evidence for low N e and genome-wide relaxed purifying selection when compared to solitary species (Galtier et al 2018;Kapheim et al 2015;Romiguier et al 2014). Future studies using both polymorphism data and divergence data will be necessary to further tease apart the contribution of elevated positive selection and relaxed purifying selection (Yang & Bielawski 2000;Nielsen 2005) to spider genome evolution.…”