Genomic islands of differentiation are associated with introgression and show heterogeneous evolutionary histories in red wood ants

Genomic differentiation between closely related species is often concentrated in discrete genomic islands, making the evolutionary processes underlying these heterogeneous genomic landscapes a major focus of evolutionary genomics. While divergent selection and recombination rate variation have received considerable attention, the contribution of introgression following hybridization remains poorly understood. Here, we investigated this question in three naturally hybridizing red wood ant species (Formica rufa, F. polyctena and F. aquilonia). Using whole genomes, we combined analyses of genetic differentiation, topology weighting, introgression and local population structure to identify genomic windows showing both elevated differentiation between the sister species F. rufa and F. polyctena and signatures of introgression between F. polyctena and F. aquilonia. All such genomic windows displayed local population structure markedly different from the genome-wide pattern, allowing us to delineate 17 introgressed genomic islands of differentiation. Bayesian phylogenetic analyses showed that these islands consistently grouped F. aquilonia with F. polyctena, but revealed substantial heterogeneity in their relative coalescence depths. This variation was unrelated to island size, introgression intensity, absolute sequence divergence or nucleotide diversity. Our results demonstrate an association between genomic differentiation and introgression in a species complex and reveal heterogeneity in the evolutionary histories of introgressed genomic islands of differentiation. More broadly, our study illustrates how integrating genomic differentiation, introgression, local genealogies and coalescence analyses can help reconstruct the evolutionary origins of genomic islands of differentiation.