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。在加拿大西海岸外的海达瓜依群岛（Haida Gwaii archipelago）的湖泊中，刺鱼发生了显著的本地辐射演化，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。为阐明该辐射演化事件的历史背景，我们对100余个种群的三棘刺鱼开展了遗传变异检测，共覆盖超过1000个单核苷酸多态性（single nucleotide polymorphism, SNP）位点。这些SNP位点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位点。基于均匀分布的SNP位点所构建的系统地理格局，与此前在两个高度分化的线粒体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系统发育树显示出极强的流域内种群聚类特征，且不同流域在树中以深层的短分支相互分隔。尽管部分独立水系间存在潜在的遗传联系，但该数据结果与多数流域的独立殖民演化假说相符。这一结果支持了此前的假说：流域间观察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独立出现在多个不同的演化支系中。在整个群岛范围内，我们观察到多个全球尺度上海洋-淡水种群分化的基因组区域（如EDA、钠钾ATP酶（Na/K ATPase））所标记的淡水适应性候选变异位点均经历了反复的正向选择。在河口生境中，可同时高频检测到海洋型和淡水型的等位基因变异。我们同时还发现，部分淡水湖泊（尤其是保留完整侧骨板的种群所在湖泊）中存在典型的海洋型等位基因。本研究结果为三棘刺鱼在冰期后淡水生境的殖民演化过程提供了普适性模型，同时也彰显了全基因组SNP数据集在解析近期适应性分化的格局与机制方面的巨大潜力。