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.

Barriers to gene flow are best studied where divergent populations are in contact, and studies of single-taxon hybrid zones have generated important knowledge about the nature of reproductive barriers.Marine environments, earlier considered to host unstructured species due to high connectivity, offer multispecies contact zones structured by simple physical gradients (e.g., salinity) ideal for comparative studies of divergence and speciation.Overlapping contact zones offer possibilities for comparison of barriers among species of various taxa, life histories, and demographic backgrounds and to test the role of species-specific traits in the formation and function of barriers.Combining genome scans and demographic modelling, barrier regions in the genome can be located and barrier origin traced. With genetic maps, inversions that affect recombination rate (and hence gene flow) can be identified.