Geographic isolation, natural selection, and demographic history interact to shape genomic divergence, yet their combined effects in island endemics remain poorly understood. We investigated the continental Euptelea pleiosperma and the island endemic E. polyandra using whole-genome resequencing of 119 and 50 individuals, respectively, providing a direct comparison of evolutionary outcomes under contrasting demographic and environmental contexts. The two species diverged in the Late Miocene (similar to 6.4 Ma), broadly coinciding with the separation of the Japanese Archipelago. Genome-wide divergence exhibited a highly heterogeneous landscape, with discrete genomic islands shaped by divergent sorting of ancient polymorphisms and divergence hitchhiking in low-recombination regions. These islands are enriched for positively selected genes related to flowering, stress responses, and climatic adaptation. Compared with continental lineages, the island endemic exhibited markedly reduced genetic diversity, elevated inbreeding, and higher genetic load, reflecting weakened purifying selection under repeated bottlenecks. Ecological niche modeling and Gradient Forest analyses further revealed severe habitat contraction and substantial genetic-environment mismatches for E. polyandra under future warming scenarios. Together, our findings provide an integrated genomic framework for understanding continental-island species evolution and highlight the heightened vulnerability of island endemics to climate change, thereby offering crucial insights into the conservation of their genetic diversity and adaptive potential.
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