Spatiotemporal genomic patterns of Quercus gilva: decoupling historical isolation from contemporary environmental adaptation

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Abstract
The interplay between historical biogeography and environmental selection shapes the genetic architecture of species; however, their relative contributions in widespread and ecologically important tree species remain poorly understood. In the Sino-Japanese Floristic Region, the East China Sea has alternately acted as a barrier and a corridor during glacial-interglacial cycles, influencing species isolation and contact. However, the extent to which these historical dynamics, along with environmental gradients, have driven adaptive evolution in dominant forest trees remains unresolved. In the present study, we integrated phylogeographic reconstruction and landscape genomics based on whole-genome resequencing data from 171 individuals across 35 populations to investigate the evolutionary history and adaptive mechanisms of Quercus gilva, a keystone evergreen oak, in East Asian subtropical forests. Population genomic analyses revealed two deeply divergent genetic groups: the China group and the Japan–Korea group, and demographic modeling indicated that their divergence dates back to the Miocene epoch. The relatively high genomic diversity of Q. gilva may result from the absence of severe genetic bottlenecks throughout its evolutionary history, multiple microrefugia during the glacial periods, and postglacial secondary contact. Notably, Quaternary glacial cycles repeatedly facilitated gene flow and admixture between these groups via exposed land bridges. Landscape genomic analyses further demonstrated that adaptive divergence in Q. gilva is shaped by both geographic isolation and environmental gradients, with annual precipitation emerging as the primary climatic driver. This study provides a genome-wide perspective on how historical biogeography and environmental selection interact to shape the genetic architecture of a dominant subtropical evergreen forest species, offering novel insights into the evolutionary dynamics and adaptive evolution across East Asian biodiversity hotspots.

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