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.

对于具有广泛扩散能力且种群规模波动的海洋无脊椎动物而言，厘清自然选择、基因流（gene flow）与遗传漂变（genetic drift）之间的动态平衡颇具挑战。潮间带滨螺——黑瘤滨螺（Chlorostoma funebralis）具有浮游幼虫（planktonic larvae）阶段，此前基于线粒体DNA多态性（mtDNA polymorphism）的相关研究未发现该物种存在遗传种群结构。尽管如此，近期研究却证实，美国加利福尼亚州北部与南部的该滨螺种群在热耐受性以及应对热胁迫的转录组响应层面存在显著差异。为深入解析驱动适应性分化的核心动态机制，本研究采用双酶切限制性位点相关DNA测序（double digest restriction site-associated DNA sequencing, ddRAD）技术，对采自加州北部3个、南部3个采样点的黑瘤滨螺（每个种群15个个体）进行测序，最终在全基因组范围内筛选得到1861个高质量单核苷酸多态性（single nucleotide polymorphism, SNP）位点。若将所有SNP位点纳入整体分析，则未检测到种群或地理区域间存在遗传分化（平均固定分化指数（FST）= 0.0042）。不过，通过离群位点检测分析，共发现34个疑似受趋异选择的位点；基于这些离群位点的群体结构分析与SNP系统发育树分析均证实，不同地理区域的种群间存在显著遗传分化。其中3个离群位点已被证实或推测参与应激颗粒（stress granule）形成过程——这是一类针对热胁迫等环境胁迫的典型应激响应机制。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的基础表达水平更高这一结果，本研究结果进一步表明，热胁迫是驱动黑瘤滨螺种群适应性分化的强选择压力。总体而言，本研究加深了学界对限制海洋生物局部适应性的关键因素的认知，同时也证实：即便对于拥有浮游幼虫阶段的海洋物种而言，由生态过程驱动的强遗传分化仍可在功能相关位点上发生。