Parallel genetic divergence among coastal-marine ecotype pairs of European anchovy explained by differential introgression after secondary contact

Ecophenotypic differentiation among replicate ecotype pairs within a species complex is often attributed to independent outcomes of parallel divergence driven by adaptation to similar environmental contrasts. However, the extent to which parallel phenotypic and genetic divergence patterns have emerged independently is increasingly questioned by population genomic studies. Here, we document the extent of genetic differentiation within and among two geographic replicates of the coastal and marine ecotypes of the European anchovy (Engraulis encrasicolus) gathered from Atlantic and Mediterranean locations. Using a genome-wide data set of RAD-derived SNPs, we show that habitat type (marine vs. coastal) is the most important component of genetic differentiation among populations of anchovy. By analysing the joint allele frequency spectrum of each coastal-marine ecotype pair, we show that genomic divergence patterns between ecotypes can be explained by a postglacial secondary contact following a long period of allopatric isolation (c. 300 kyrs). We found strong support for a model including heterogeneous migration among loci, suggesting that secondary gene flow has eroded past differentiation at different rates across the genome. Markers experiencing reduced introgression exhibited strongly correlated differentiation levels among Atlantic and Mediterranean regions. These results support that partial reproductive isolation and parallel genetic differentiation among replicate pairs of anchovy ecotypes are largely due to a common divergence history prior to secondary contact. They moreover provide comprehensive insights into the origin of a surprisingly strong fine-scale genetic structuring in a high gene flow marine fish, which should improve stock management and conservation actions.

物种复合群（species complex）内重复生态型对之间的生态表型分化（ecophenotypic differentiation）通常被归因于适应相似环境差异所驱动的平行分化的独立演化结果。然而，平行表型与遗传分化模式究竟在多大程度上能够独立形成，这一问题日益受到群体基因组学研究的质疑。本研究针对采自大西洋与地中海海域的欧洲鳀（Engraulis encrasicolus）海岸与海洋生态型的2组地理重复样本，解析了其种群内部及种群间的遗传分化程度。借助全基因组范围的限制性位点相关DNA测序（Restriction-site Associated DNA sequencing, RAD）衍生的单核苷酸多态性（Single Nucleotide Polymorphism, SNP）数据集，我们证实生境类型（海洋vs. 海岸）是鳀鱼种群间遗传分化的最核心驱动因素。通过分析每一组海岸-海洋生态型对的联合等位基因频率谱（Joint Allele Frequency Spectrum, JAFS），我们发现生态型间的基因组分化模式可通过一段长达约30万年的异域隔离后发生的冰期后二次接触得以解释。我们获得了强烈支持‘位点间迁移率存在异质性’模型的证据，这表明二次基因流以不同速率侵蚀了基因组内既往的分化水平。在大西洋与地中海区域中，经历基因渐渗减弱的遗传标记均表现出高度相关的分化程度。上述结果证实，鳀鱼重复生态型对之间存在的部分生殖隔离与平行遗传分化，在很大程度上源于二次接触前共有的分化历史。此外，本研究还为这类高基因流海水鱼类中出乎意料的精细尺度强遗传结构的起源提供了全面解析，相关成果可优化渔业种群管理与保护行动。