Evidence of neutral and adaptive genetic divergence between European trout populations sampled along altitudinal gradients

Species with a wide geographical distribution are often composed of distinct subgroups which may be adapted to their local environment. European trout (Salmo trutta species complex) provide an example of such a complex consisting of several genetically and ecologically distinct forms. However, trout populations are strongly influenced by human activities, and it is unclear to what extent neutral and adaptive genetic differences have persisted. We sampled 30 Swiss trout populations from heterogeneous environments along replicated altitudinal gradients in three major European drainages. More than 850 individuals were genotyped at 18 microsatellite loci which included loci diagnostic for evolutionary lineages and candidate markers associated with temperature tolerance, reproductive timing and immune defence. We find that the phylogeographic structure of Swiss trout populations has not been completely erased by stocking. Distinct genetic clusters corresponding to the different drainages could be identified, although nonindigenous alleles were clearly present, especially in the two Mediterranean drainages. We also still detected neutral genetic differentiation within rivers which was often associated with the geographical distance between populations. Five loci showed evidence of divergent selection between populations with several drainage-specific patterns. Lineage-diagnostic markers, a marker linked to a quantitative trait locus for upper temperature tolerance in other salmonids and a marker linked to the major histocompatibility class I gene were implicated in local adaptation and some patterns were associated with altitude. In contrast, tentative evidence suggests a signal of balancing selection at a second immune relevant gene (TAP2). Our results confirm the persistence of both neutral and potentially adaptive genetic differences between trout populations in the face of massive human-mediated dispersal.

地理分布范围广阔的物种通常由多个适配本地生境的独特亚群所构成。欧洲鲑（Salmo trutta物种复合群）便是这类由多个遗传与生态特征均具独特性的类群所组成的复合群典型范例。然而，鲑鱼种群深受人类活动的强烈影响，目前尚不清楚中性遗传差异与适应性遗传差异在多大程度上得以保留。本研究沿三条主要欧洲流域的重复海拔梯度异质生境中，采样了30个瑞士鲑鱼种群；我们对850余尾个体的18个微卫星位点（microsatellite loci）进行了基因分型，这些位点包含用于区分进化支系的诊断位点，以及与温度耐受、繁殖时序和免疫防御相关的候选标记。研究发现，瑞士鲑鱼种群的系统地理结构（phylogeographic structure）并未因人工放流而完全消失：尽管明显存在外来等位基因，尤其在两个地中海流域种群中，但仍可识别出对应不同流域的独特遗传聚类。此外，研究团队还检测到流域内部种群间的中性遗传分化，且该分化多与种群间的地理距离呈显著关联。五个位点显示出种群间歧化选择的信号，且存在多种流域特异性演化模式。支系诊断标记、与其他鲑科鱼类高温耐受数量性状位点（quantitative trait locus, QTL）连锁的标记，以及与主要组织相容性复合体I类（major histocompatibility class I, MHC I）基因连锁的标记，均与本地适应相关，且部分模式与海拔高度存在关联。与之相对，暂存研究证据显示，另一免疫相关基因（TAP2）存在平衡选择信号。本研究结果证实，即便面临人类介导的大规模种群扩散，瑞士鲑鱼种群间的中性遗传差异与潜在适应性遗传差异仍得以保留。