Data from: Range expansion compromises adaptive evolution in an outcrossing plant

Neutral genetic diversity gradients have long been used to infer the colonization history of species, but range expansion may also influence the efficacy of natural selection and patterns of non-synonymous polymorphism in different parts of a species’ range. Recent theory predicts both an accumulation of deleterious mutations and a reduction in the efficacy of positive selection as a result of range expansion. These signatures have been sought in a number of studies of the human range expansion out of Africa, but with contradictory results. We analyzed the polymorphism patterns of 578,125 SNPs (17,648 genes) in the European diploid plant Mercurialis annua, which expanded its range from an eastern Mediterranean refugium into western habitats with contrasted climates. Our results confirmed strong signatures of bottlenecks and revealed the accumulation of mildly to strongly deleterious mutations in range-front populations. A significantly higher number of these mutations were homozygous in individuals in range-front populations, pointing to increased genetic load and reduced fitness under a model of recessive deleterious effects. We also inferred a reduction in the number of selective sweeps in range-front versus core populations. These signatures have persisted even in a dioecious herb subject to substantial interpopulation gene flow. Our results extend support from humans to plants for theory on the dynamics of mutations under selection during range expansion, showing that colonization bottlenecks can compromise adaptive potential.

中性遗传多样性梯度（neutral genetic diversity gradients）长期以来被用于推断物种的定殖历史，但范围扩张（range expansion）也可能影响自然选择效力以及物种分布范围内不同区域的非同义多态性（non-synonymous polymorphism）模式。近期理论预测，范围扩张会同时导致有害突变（deleterious mutations）积累以及正选择（positive selection）效力下降。这类特征信号已在多项针对人类走出非洲的范围扩张研究中被探寻，但得到了相互矛盾的结果。本研究对欧洲二倍体植物一年生山靛（Mercurialis annua）的多态性模式进行了分析，共涉及578125个单核苷酸多态性（SNPs）（对应17648个基因）；该物种的分布范围从地中海东部避难所扩张至气候迥异的西部生境。研究结果证实了种群瓶颈的显著特征信号，并发现扩张前沿种群（range-front populations）中存在轻度至重度有害突变的积累。扩张前沿种群个体中携带这类突变的纯合比例显著更高，这表明在隐性有害效应模型下，种群的遗传负荷（genetic load）升高且适合度（fitness）下降。我们还推断，相较于核心种群（core populations），扩张前沿种群的选择性清除（selective sweeps）事件数量有所减少。即使在存在大量种群间基因交流（interpopulation gene flow）的雌雄异株草本植物中，这类特征信号依然存在。本研究将此前基于人类的研究结论拓展至植物类群，验证了范围扩张过程中选择下的突变动态理论，表明定殖瓶颈（colonization bottlenecks）会削弱物种的适应性潜力（adaptive potential）。