Data from: Phylogeography and adaptation genetics of stickleback from the Haida Gwaii archipelago revealed using genome-wide SNP genotyping

Threespine stickleback populations are model systems for studying adaptive evolution and the underlying genetics. In lakes on the Haida Gwaii archipelago (off western Canada), stickleback have undergone a remarkable local radiation and show phenotypic diversity matching that seen throughout the species distribution. To provide a historical context for this radiation, we surveyed genetic variation at >1000 single nucleotide polymorphism (SNP) loci in stickleback from over 100 populations. SNPs included markers evenly distributed throughout genome and candidate SNPs tagging adaptive genomic regions. Based on evenly distributed SNPs, the phylogeographic pattern differs substantially from the disjunct pattern previously observed between two highly divergent mtDNA lineages. The SNP tree instead shows extensive within watershed population clustering and different watersheds separated by short branches deep in the tree. These data are consistent with separate colonizations of most watersheds, despite underlying genetic connections between some independent drainages. This supports previous suppositions that morphological diversity observed between watersheds has been shaped independently, with populations exhibiting complete loss of lateral plates and giant size each occurring in several distinct clades. Throughout the archipelago, we see repeated selection of SNPs tagging candidate freshwater adaptive variants at several genomic regions differentiated between marine–freshwater populations on a global scale (e.g. EDA, Na/K ATPase). In estuarine sites, both marine and freshwater allelic variants were commonly detected. We also found typically marine alleles present in a few freshwater lakes, especially those with completely plated morphology. These results provide a general model for postglacial colonization of freshwater habitat by sticklebacks and illustrate the tremendous potential of genome-wide SNP data sets hold for resolving patterns and processes underlying recent adaptive divergences.

三棘刺鱼（Threespine stickleback）种群是研究适应性进化及其潜在遗传机制的经典模式系统。在加拿大西部海域的海达瓜依群岛（Haida Gwaii archipelago）的湖泊中，刺鱼经历了显著的本地辐射进化，其表型多样性可与该物种全球分布范围内的表型多样性相媲美。为了为这一辐射进化过程提供历史背景，我们对100余个种群的刺鱼开展了遗传变异筛查，共覆盖超过1000个单核苷酸多态性（single nucleotide polymorphism, SNP）位点。这些SNP既包含均匀分布于全基因组的标记位点，也包含用于标记适应性基因组区域的候选SNP。基于均匀分布的SNP数据，其揭示的系统地理格局与此前在两种高度分化的线粒体DNA（mitochondrial DNA, mtDNA）谱系间观察到的间断格局存在显著差异。与之相反，SNP系统发育树显示种群聚类广泛发生在同一流域内部，且不同流域之间以系统树深处的短分支相互分隔。这些数据与多数流域的独立拓殖事件相一致，尽管部分独立水系间存在潜在的遗传联系。这一结果支持了此前的假说：不同流域间观测到的形态多样性是独立演化形成的——例如完全丢失侧骨板以及体型巨型的种群，均分别出现在多个独立的演化支（clades）中。在整个群岛范围内，我们观测到针对多个在全球尺度海水-淡水种群间存在分化的基因组区域，靶向其候选淡水适应性变异的SNP位点受到了反复选择，例如EDA基因、钠钾ATP酶（Na/K ATPase）相关位点。在河口生境中，海洋和淡水两种等位基因变异均常被检测到。我们还发现，少数淡水湖泊（尤其是具有完全骨板表型的湖泊）中普遍存在典型的海洋等位基因。这些研究结果为刺鱼冰期后拓殖淡水生境提供了通用模型，同时也阐明了全基因组SNP数据集在解析近期适应性分化背后的模式与过程方面所具备的巨大潜力。