The impact of selection, gene flow and demographic history on heterogeneous genomic divergence: threespine sticklebacks in divergent environments

Heterogeneous genomic divergence between populations may reflect selection, but should also be seen in conjunction with gene flow and drift, particularly population bottlenecks. Marine and freshwater threespine stickleback (Gasterosteus aculeatus) populations often exhibit different lateral armor plate morphs. Moreover, strikingly parallel genomic footprints across different marine-freshwater population pairs are interpreted as parallel evolution and gene reuse. Nevertheless, in some geographic regions like the North Sea and Baltic Sea different patterns are observed. Freshwater populations in coastal regions are often dominated by marine morphs, suggesting that gene flow overwhelms selection, and genomic parallelism may also be less pronounced. We used RAD sequencing for analyzing 28,888 SNPs in two marine and seven freshwater populations in Denmark, Europe. Freshwater populations represented a variety of environments: river populations accessible to gene flow from marine sticklebacks and large and small isolated lakes with and without fish predators. Sticklebacks in an accessible river environment showed minimal morphological and genome-wide divergence from marine populations, supporting the hypothesis of gene flow overriding selection. Allele frequency spectra suggested bottlenecks in all freshwater populations, and particularly two small lake populations. However, genomic footprints ascribed to selection could nevertheless be identified. No genomic regions were consistent freshwater-marine outliers, and parallelism was much lower than in other comparable studies. Two genomic regions previously described to be under divergent selection in freshwater and marine populations were outliers between different freshwater populations. We ascribe these patterns to stronger environmental heterogeneity among freshwater populations in our study as compared to most other studies, although the demographic history involving bottlenecks should also be considered in the interpretation of results.

种群间的异质性基因组分化既可反映选择压力的作用，同时也会伴随基因流与遗传漂变过程出现，尤以种群瓶颈效应（population bottlenecks）最为显著。海洋与淡水三棘刺鱼（Gasterosteus aculeatus）种群通常表现出不同的侧骨板形态型。此外，不同海洋-淡水种群配对间存在的显著平行基因组印记（parallel genomic footprints），通常被解读为平行进化与基因复用（gene reuse）的结果。然而在北海、波罗的海等部分海域，却观测到了截然不同的模式。沿海区域的淡水种群通常以海洋型刺鱼为主，这表明基因流的作用盖过了选择压力，且基因组平行性也往往较弱。本研究采用RAD测序（RAD sequencing）技术，对欧洲丹麦境内的2个海洋种群与7个淡水种群的28888个单核苷酸多态性位点（SNPs）进行了分析。本次研究涉及的淡水种群涵盖多种生境类型：可与海洋刺鱼发生基因流的河流种群，以及分别存在/不存在鱼类捕食者的大型、小型孤立湖泊种群。处于可发生基因交流的河流生境中的刺鱼，其形态学与全基因组分化程度均与海洋种群极为接近，这支持了"基因流作用盖过选择压力"的假说。等位基因频率谱分析显示，所有淡水种群均存在瓶颈效应，其中2个小型湖泊种群的瓶颈效应尤为显著。尽管如此，本研究仍成功鉴定出了归因于选择作用的基因组印记。未发现淡水-海洋种群间存在一致的基因组分化异常区域，且基因组平行性远低于其他同类研究。此前被报道在淡水与海洋种群间受歧化选择作用的2个基因组区域，在不同淡水种群间反而呈现出分化异常特征。本研究将上述模式归因于本次研究中淡水种群间的生境异质性强于多数同类研究，不过在解读结果时也应纳入涉及瓶颈效应的种群历史动态因素。