Linked selection and recombination rate generate both shared and lineage-specific genomic islands of divergence in two independent Quercus species pairs

A fundamental question in speciation genomics is how evolutionary processes shape the genomic landscape of differentiation between species. Regions of elevated differentiation, referred to as genomic islands, could be shared among closely related species (shared islands) or specific to a lineage (lineage-specific islands). Shared islands are typically assumed to result from background selection. However, simulations and empirical studies have suggested that positive selection contributes to both shared and lineage-specific islands. Here, we utilized comparative population genomics to examine the contributions of different evolutionary processes to patterns of genetic differentiation when gene flow and incomplete lineage sorting are minimal. We used whole-genome resequencing data for 135 individuals from four oak species, including two independent species pairs, Quercus variabilis Blume and Quercus acutissima Carruth. in the subgenus Cerris, and Quercus dentata Thunb. and Quercus griffithii Hook.f. & Thomson ex Miq. in the subgenus Quercus. We found that both shared and subgenus-specific islands were caused by positive selection, including selective sweeps in current populations and in their most recent common ancestors. Moreover, the recombination rate was a better predictor of genomic differentiation than gene density. Overall, our results reveal that recombination and positive selection impacted genomic differentiation considerably and provide a more precise grasp of how genomic islands formed in Quercus.