Ecotype formation in the European anchovy fuelled by structural variants of different origins and genetic interactions with a southern lineage

The speciation of ecotypes can unfold in diverse ways and likely depends on multiple processes. The variants involved in ecotype divergence can include new mutations as well as older allelic variation that evolved in different contexts. Among the different types of variants that can contribute to reproductive isolation between ecotypes, structural variants (SVs) represent likely candidates due to their ability to protect divergent haplotypes from recombination and gene flow. The European anchovy (Engraulis encrasicolus) is known to be subdivided into marine and coastal ecotypes, and their divergence shows patterns that are consistent with SVs. Here, we present the first genome-scale study investigating genetic structure in the E. encrasicolus species complex. We generated a reference genome and produced whole-genome resequencing data for anchovies from the North-East Atlantic and Mediterranean Sea, as well as from South Africa. We complemented this approach with the analysis of RAD-seq data in order to study ecotypic structure across the entire distribution range. We found that genetic diversity is not only characterised by the presence of two genetic clusters, namely the marine and coastal ecotypes, but also by a third ancestry which corresponds to a southern Atlantic lineage. This lineage occurs off South Africa but also in southern Morocco and the Canary Islands, and shows a gradient of admixture with northern populations nearing the Atlantic-Mediterranean transition zone. Genomic landscapes of differentiation showed evidence for large regions of high linkage disequilibrium, likely representing SVs that differentiate the three anchovy lineages. We found evidence that three of the SVs contributing to the gene flow barrier between ecotypes originated in the southern lineage, suggesting that the coastal and southern lineages have a partly shared evolutionary history. In addition to these barriers, three other SVs contributing to ecotype differentiation appear to have evolved in situ. Anchovies thus present an interesting case for the study of ecotype speciation, since the barriers involved in reproductive isolation have different origins and have partly diverged in geographic isolation.