Linked selection, ancient polymorphism, and ecological adaptation shape the genomic landscape of divergence in Quercus dentata

Abstract

AbstractMultiple evolutionary forces contribute to heterogeneous genomic landscapes; however, disentangling their relative contributions is challenging. We sampled nine populations across the distribution of Quercus dentata, a dominant forest tree in East Asia, and used whole‐genome sequencing data to investigate mechanisms underlying divergence. We identified two genetic groups (north and south) that diverged ~1.84 million years ago, consistent with the uplift of the Qinling Mountains during the Pleistocene. The north group experienced a bottleneck during the middle–late Pleistocene and expanded from multiple refugia. The south group experienced a more severe bottleneck and showed high population differentiation, probably due to long‐term isolation and habitat fragmentation. We detected genomic islands with elevated relative differentiation (FST) scattered across the genome. Among these, 65.9% showed reduced absolute divergence (dXY) consistent with linked selection, while the remaining (34.1%) showed elevated dXY suggestive of divergent sorting of ancient polymorphisms. The recombination rate in genomic islands was lower than background, suggesting the importance of genome structure in shaping the genomic landscape. We detected 108 single nucleotide polymorphisms significantly associated with environmental factors, 12 of which clustered in a region of ~500 kb. This region showed multiple signals of positive selection in the north group, including the enrichment of XP‐extended haplotype homozygosity scores, an elevated population branch statistic, and an excess of high‐frequency derived alleles. In addition, we found that linkage disequilibrium was low and derived haplotypes declined rapidly in this region, indicating selection on standing variation. Our results clarify the evolutionary processes driving genomic divergence in Q. dentata.