Haenel Quiterie, Roesti Marius, Moser Dario, MacColl Andrew D C, Berner Daniel
Department of Environmental Sciences, Zoology University of Basel 4051 Basel Switzerland.
Biodiversity Research Centre and Zoology Department University of British Columbia Vancouver British Columbia V6T 1Z4 Canada.
Evol Lett. 2019 Jan 23;3(1):28-42. doi: 10.1002/evl3.99. eCollection 2019 Feb.
Genomic studies of parallel (or convergent) evolution often compare multiple populations diverged into two ecologically different habitats to search for loci repeatedly involved in adaptation. Because the shared ancestor of these populations is generally unavailable, the source of the alleles at adaptation loci, and the direction in which their frequencies were shifted during evolution, remain elusive. To shed light on these issues, we here use multiple populations of threespine stickleback fish adapted to two different types of derived freshwater habitats-basic and acidic lakes on the island of North Uist, Outer Hebrides, Scotland-and the present-day proxy of their marine ancestor. In a first step, we combine genome-wide pooled sequencing and targeted individual-level sequencing to demonstrate that ecological and phenotypic parallelism in basic-acidic divergence is reflected by genomic parallelism in dozens of genome regions. Exploiting data from the ancestor, we next show that the acidic populations, residing in ecologically more extreme derived habitats, have adapted by accumulating alleles rare in the ancestor, whereas the basic populations have retained alleles common in the ancestor. Genomic responses to selection are thus predictable from the ecological difference of each derived habitat type from the ancestral one. This asymmetric sorting of standing genetic variation at loci important to basic-acidic divergence has further resulted in more numerous selective sweeps in the acidic populations. Finally, our data suggest that the maintenance in marine fish of standing variation important to adaptive basic-acidic differentiation does not require extensive hybridization between the marine and freshwater populations. Overall, our study reveals striking genome-wide determinism in both the loci involved in parallel divergence, and in the direction in which alleles at these loci have been selected.
对平行（或趋同）进化的基因组研究通常会比较多个分化进入两种生态不同栖息地的种群，以寻找反复参与适应性进化的基因座。由于这些种群的共同祖先通常难以确定，适应性基因座上等位基因的来源以及它们在进化过程中频率发生变化的方向仍然难以捉摸。为了阐明这些问题，我们在这里使用了多群三刺鱼，它们适应了两种不同类型的衍生淡水栖息地——苏格兰外赫布里底群岛北尤伊斯特岛上的碱性湖和酸性湖，以及它们现代的海洋祖先代表。第一步，我们结合全基因组混合测序和靶向个体水平测序，以证明碱性 - 酸性分化中的生态和表型平行性反映在数十个基因组区域的基因组平行性上。利用来自祖先的数据，我们接下来表明，生活在生态上更为极端的衍生栖息地的酸性种群，通过积累祖先中罕见的等位基因而实现了适应，而碱性种群则保留了祖先中常见的等位基因。因此，从每个衍生栖息地类型与祖先栖息地的生态差异可以预测基因组对选择的反应。在对碱性 - 酸性分化至关重要的基因座上，这种现存遗传变异的不对称分选进一步导致酸性种群中出现更多的选择性清除。最后，我们的数据表明，海洋鱼类中对适应性碱性 - 酸性分化至关重要的现存变异的维持并不需要海洋和淡水种群之间进行广泛的杂交。总体而言，我们的研究揭示了在参与平行分化的基因座以及这些基因座上等位基因被选择的方向上，全基因组层面都存在显著的决定性。
