The contribution of ancient admixture to reproductive isolation between European sea bass lineages

Understanding how new species arise through the progressive establishment
of reproductive isolation barriers between diverging populations is a
major goal in Evolutionary Biology. An important result of speciation
genomics studies is that genomic regions involved in reproductive
isolation frequently harbor anciently diverged haplotypes that predate the
reconstructed history of species divergence. The possible origins of these
old alleles remain much debated, as they relate to contrasting mechanisms
of speciation that are not yet fully understood. In the European sea bass
(Dicentrarchus labrax), the genomic regions involved in reproductive
isolation between Atlantic and Mediterranean lineages are enriched for
anciently diverged alleles of unknown origin. Here, we used
haplotype-resolved whole-genome sequences to test whether divergent
haplotypes could have originated from a closely related species, the
spotted sea bass (Dicentrarchus punctatus). We found that an ancient
admixture event between D. labrax and D. punctatus is responsible for the
presence of shared derived alleles that segregate at low frequencies in
both lineages of D. labrax. An exception to this was found within regions
involved in reproductive isolation between the two D. labrax lineages. In
those regions, archaic tracts originating from D. punctatus locally
reached high frequencies or even fixation in Atlantic genomes but were
almost absent in the Mediterranean. We showed that the ancient admixture
event most likely occurred between D. punctatus and the D. labrax Atlantic
lineage, while Atlantic and Mediterranean D. labrax lineages were
experiencing allopatric isolation. Our results suggest that local adaptive
introgression and/or the resolution of genomic conflicts provoked by
ancient admixture have probably contributed to the establishment of
reproductive isolation between the two D. labrax lineages.