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

Abstract

Multiple 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 (F ST ) scattered across the genome. Among these, 65.9% showed reduced absolute divergence (d XY ) consistent with linked selection, while the remaining (34.1%) showed elevated d XY 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.

Genomic signals of local adaptation and hybridization in Asian white birch

“…Within our B. platyphylla samples, we found three genetic clusters with some admixed individuals between them. The three clusters seem to mirror similar phylogeographic breaks in many other plant species (Bai et al, 2016; Fan et al, 2013; Ye et al, 2017; Zhou et al, 2022) and our interpretation of B. platyphylla population structure is similar to that of Chen and Lou (2019). Our fastsimcoal results suggest that the three B. platyphylla populations exchanged genetic material soon after their divergence and recently but endured a long period of isolation in between these contacts (Figure 3d).…”

Genomic vulnerability to climate change in Quercus acutissima, a dominant tree species in East Asian deciduous forests

“…These results indicate a pattern of IBE generated by adaptation to local environments (Wang & Bradburd, 2014). The pervasive signatures of local adaptation and their influences on the spatial distribution of genetic variation have been well documented in forest trees (Lind et al, 2018; Savolainen et al, 2007; Xia et al, 2018; Zhao et al, 2020; Zhou, Shi, et al, 2022).…”

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

“…In total, 55 natural populations (135 individuals) were sampled, covering the main distribution of the four oak species in China, including 18 populations (34 individuals) of Quercus acutissima , 24 populations (47 individuals) of Quercus variabilis , nine populations (38 individuals) of Quercus dentata , and four populations (16 individuals) of Quercus griffithii (Table ). Whole‐genome sequencing data for these samples were obtained from previous publications (Liang et al, 2022; Zhou et al, 2022a), with the exception of eight Q. griffithii individuals sequenced in this study. For these new samples, young leaves were collected from each individual and immediately dried in silica gel for DNA isolation.…”

“…Interspecific hybridization is prevalent within sections of Quercus and less common between sections and subgenera (Crowl et al, 2020; Hipp et al, 2020; Li et al, 2021; Fu et al, 2022; Zhou et al, 2022b). Previous studies have suggested that linked selection has played a major role in shaping the heterogeneous genomic landscape of oak species (Gao et al, 2021; Liang et al, 2022; Zhou et al, 2022a). Here, we use comparative population genomics approaches to understand the relative contributions of different types of linked selection to the formation of shared and lineage‐specific islands.…”