Speciation is a complex process that leads to the progressive establishment of reproductive isolation barriers between diverging populations. Genome-wide comparisons between closely related species have revealed the existence of heterogeneous divergence patterns, dominated by genomic islands of increased divergence supposed to contain reproductive isolation loci. However, this divergence landscape only provides a static picture of the dynamic process of speciation, during which confounding mechanisms unrelated to speciation can interfere. Here we use haplotype-resolved whole-genome sequences to identify the mechanisms responsible for the formation of genomic islands between Atlantic and Mediterranean sea bass lineages. Local ancestry patterns show that genomic islands first emerged in allopatry through linked selection acting on a heterogeneous recombination landscape. Then, upon secondary contact, preexisting islands were strongly remolded by differential introgression, revealing variable fitness effects among regions involved in reproductive isolation. Interestingly, we find that divergent regions containing ancient polymorphisms conferred the strongest resistance to introgression.
The speciation process tends to generate ‘genomic islands’ of increased divergence. Here, the authors use haplotype–resolved whole-genome sequences of European sea bass lineages to infer divergence history and show that linked selection generated genomic islands that resist introgression at secondary contact.