Contrasting Roles of the Multiple Seas in East Asia on Population Divergence of Smilax sieboldii (Smilacaceae)

Multiple seas in East Asia have played distinct roles during the Quaternary climatic cycles, which have repeatedly isolated and reconnected temperate forest species, while it remains unclear whether their roles differ. In this study, we used Smilax sieboldii, a widely distributed species along the eastern coast of East Asia, to simultaneously evaluate the roles of multiple seas, including the East China Sea, the Yellow-Bohai Sea, the Korea-Tsushima Strait, and the Taiwan Strait, as geographic barriers and dispersal corridors during historical sea-level fluctuations. We employed Bayesian clustering analysis and demographic simulations to elucidate the genetic structure and evolutionary history. The effects of spatial or environmental differences on population structure were examined through isolation by distance (IBD) and isolation by environment (IBE) tests. Further, genetic differentiation and gene flow were used as indicators to assess the roles of different seas as barriers or corridors. A pronounced phylogeographic structure was observed in S. sieboldii, with populations divided into three distinct gene pools separated by the East China Sea and the Korea-Tsushima Strait, accompanied by significant genetic admixture at the lineage boundaries. The lineage divergence occurred during the early Quaternary, while secondary contact began in the most recent interglacial period. During population differentiation, the East China Sea and the Korea-Tsushima Strait acted as effective geographic barriers, whereas the Taiwan Strait and the Yellow-Bohai Sea functioned more as dispersal corridors and facilitated greater gene flow. Meanwhile, IBD rather than IBE explained the population structure of S. sieboldii. To conclude, the phylogeographic patterns of S. sieboldii resulted from population isolation and admixture due to sea-level fluctuations since the Pleistocene, and the spatial scale of a sea largely determined its ecological role among the multi-sea systems. These findings improved our understanding of how paleoclimate changes and geological transformations have shaped the speciation and diversification of temperate forest species in East Asia.