Data from: Genomic evidence for ecological divergence against a background of population homogeneity in the marine snail Chlorostoma funebralis

The balance between natural selection, gene flow, and genetic drift is difficult to resolve in marine invertebrates with extensive dispersal and fluctuating population sizes. The intertidal snail Chlorostoma funebralis has planktonic larvae and previous work using mtDNA polymorphism reported no genetic population structure. Nevertheless, recent studies have documented differences in thermal tolerance and transcriptomic responses to heat stress between northern and southern California, USA, populations. To gain insight into the dynamics influencing adaptive divergence, we used double digest restriction site-associated DNA (ddRAD) sequencing to identify 1861 genome-wide, quality filtered single nucleotide polymorphism (SNP) loci for C. funebralis collected from three northern and three southern California sites (15 individuals per population). Considering all SNPs, there was no evidence for genetic differentiation among populations or regions (average FST = 0.0042). However, outlier tests revealed 34 loci putatively under divergent selection between northern and southern populations, and structure and SNP tree analyses based on these outliers show clear genetic differentiation between geographic regions. Three of these outliers are known or hypothesized to be involved in stress granule formation, a response to environmental stress such as heat. Combined with previous work that found thermally tolerant southern populations show high baseline expression of stress response genes, these results further suggest that thermal stress is a strong selective pressure across C. funebralis populations. Overall, this study increases our understanding of the factors constraining local adaptation in marine organisms, while suggesting that ecologically driven, strong differentiation can occur at relevant loci in a species with planktonic larvae.在具备广泛扩散能力且种群数量波动剧烈的海洋无脊椎动物类群中，厘清自然选择、基因流与遗传漂变之间的平衡关系极具挑战。潮间带蝾螺（Chlorostoma funebralis）拥有浮游幼虫阶段，此前基于线粒体DNA多态性开展的研究未发现其存在种群遗传结构。然而近期研究证实，美国加利福尼亚州北部与南部的该物种种群在耐热性以及热应激转录组响应方面存在显著差异。 为深入解析驱动适应性分化的动态机制，本研究采用双酶切限制性位点相关DNA测序（double digest restriction site-associated DNA, ddRAD）技术，对采自加州北部、南部各3个采样点（每个种群15个个体）的潮间带蝾螺进行测序，最终鉴定得到1861个经过质量筛选的全基因组单核苷酸多态性（single nucleotide polymorphism, SNP）位点。 对所有SNP位点的分析显示，种群或地理区域间未检测到显著遗传分化（平均F_ST = 0.0042）。但离群位点检测共筛选出34个可能受歧化选择作用的位点；基于这些位点的群体结构分析与SNP系统发育树分析结果表明，南北地理区域间存在清晰的遗传分化。其中3个离群位点已知或被推测参与应激颗粒形成——这是一类针对热应激等环境压力的细胞响应机制。结合此前研究发现的耐热性更强的南部种群其应激响应基因基础表达水平更高的结果，本研究结果进一步表明，热应激是驱动潮间带蝾螺种群分化的强选择压力。 总体而言，本研究增进了学界对限制海洋生物局部适应的各类因素的认知，同时也提示：即便在具有浮游幼虫阶段的物种中，生态驱动的强选择作用仍可在关键功能位点引发显著遗传分化。