Data from: Evolution of sociality in spiders leads to depleted genomic diversity at both population and species level

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 genome-wide 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 6-10 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 genome-wide diversity, likely to limit their evolutionary potential.

在多个动物类群中，社会性的演化涉及一系列特征，即所谓的“社会综合征（social syndrome）”，这些特征包括合作繁育、繁殖偏倚、初始雌性偏倚性比，以及从异交向近交交配系统的转变——上述因素均会降低有效种群大小（Ne）。这种社会综合征或许可通过短期收益获得选择青睐，但也伴随长期代价：Ne的降低会通过遗传漂变加剧遗传多样性的丧失，最终限制种群应对环境变化的演化潜力。为探究此类社会生活方式对遗传多样性的影响，我们采用比较性限制性位点相关DNA测序（RAD-sequencing）方法，对社会性程度、繁殖偏倚和交配系统存在差异的蜘蛛物种开展全基因组多样性评估。我们分析了3组独立的社会性近交与亚社会性异交Stegodyphus蜘蛛的姐妹物种对，以及一个亚社会性外类群的多个种群。结果显示，与亚社会性物种相比，社会性物种的杂合度及种群内多样性低6至10倍；种群人口学建模表明，社会性种群的Ne下降了10倍。物种水平的遗传多样性取决于种群分化与遗传谱系的存续能力。本研究中的种群基因组模式与高谱系更新率相符——这种更新会均质化近交种群间形成的遗传结构，最终在物种水平上耗竭遗传多样性。事实上，社会性物种的物种水平遗传多样性比亚社会性物种低5至8倍。具有这类社会综合征的物种的多次独立演化事件，均伴随严重的全基因组多样性丧失，这大概率会限制其演化潜力。