Genome-wide signatures of local selection in the panmictic European eel

Next-generation sequencing and the collection of genome-wide data allow identifying adaptive variation and footprints of directional selection. Using a large SNP data set from 259 RAD-sequenced European eel individuals (glass eels) from eight locations between 34 and 64oN, we examined the patterns of genome-wide genetic diversity across locations. We tested for local selection by searching for increased population differentiation using FST-based outlier tests and by testing for significant associations between allele frequencies and environmental variables. The overall low genetic differentiation found (FST = 0.0007) indicates that most of the genome is homogenized by gene flow, providing further evidence for genomic panmixia in the European eel. The lack of genetic substructuring was consistent at both nuclear and mitochondrial SNPs. Using an extensive number of diagnostic SNPs, results showed a low occurrence of hybrids between European and American eel, mainly limited to Iceland (5.9%), although individuals with signatures of introgression several generations back in time were found in mainland Europe. Despite panmixia, a small set of SNPs showed high genetic differentiation consistent with single-generation signatures of spatially varying selection acting on glass eels. After screening 50 354 SNPs, a total of 754 potentially locally selected SNPs were identified. Candidate genes for local selection constituted a wide array of functions, including calcium signalling, neuroactive ligand–receptor interaction and circadian rhythm. Remarkably, one of the candidate genes identified is PERIOD, possibly related to differences in local photoperiod associated with the >30° difference in latitude between locations. Genes under selection were spread across the genome, and there were no large regions of increased differentiation as expected when selection occurs within just a single generation due to panmixia. This supports the conclusion that most of the genome is homogenized by gene flow that removes any effects of diversifying selection from each new generation.

新一代测序技术与全基因组数据采集，可用于鉴定适应性变异与定向选择的印迹。本研究依托采自北纬34°至64°间8个采样点的259条经限制性位点相关DNA测序（Restriction-site Associated DNA sequencing，RAD-seq）的欧洲鳗鲡（玻璃鳗）个体的大型单核苷酸多态性（Single Nucleotide Polymorphism，SNP）数据集，分析了各采样点间的全基因组遗传多样性模式。研究通过开展基于固定指数（Fixation Index，FST）的离群值检测以寻找群体分化升高的位点，并检验等位基因频率与环境变量间的显著关联，以此检测局部选择作用。本次研究检测到整体极低的遗传分化水平（FST=0.0007），表明绝大多数基因组因基因流而实现均质化，为欧洲鳗鲡的基因组泛交（panmixia）现象提供了进一步佐证。核单核苷酸多态性与线粒体单核苷酸多态性均未呈现遗传亚结构。借助大量诊断性单核苷酸多态性位点，研究发现欧洲与美洲鳗鲡的杂交个体发生率极低，且主要集中于冰岛（占比5.9%）；尽管在欧洲大陆也发现了携带多代前基因渐渗（introgression）印迹的个体。尽管存在基因组泛交现象，但仍有少量单核苷酸多态性位点呈现出较高的遗传分化，与作用于玻璃鳗的空间异质选择的单代印迹特征相符。在对50354个单核苷酸多态性位点进行筛选后，共计鉴定出754个可能受局部选择作用的位点。受局部选择作用的候选基因功能多样，涵盖钙信号通路、神经活性配体-受体相互作用以及昼夜节律等多个生物学过程。值得注意的是，本次鉴定出的候选基因中包含PERIOD基因，其可能与各采样点间超过30°纬度差异所带来的局部光周期差异相关。受选择作用的基因遍布于整个基因组，并未出现预期的高分化大片段区域——这一结果符合泛交背景下选择仅作用于单代的情况。本研究结果进一步佐证了如下结论：绝大多数基因组通过基因流实现均质化，从而清除了每一代新个体中所产生的歧化选择效应。