Population genomics and phylogeography of Actaea vaginata reveal four geographically structured lineages and their demographic history in the Hengduan Mountains region

The widespread distribution of Actaea vaginata across the Hengduan Mountains (HDM), despite strong environmental and topographic heterogeneity, makes it an ideal system for investigating its population genetic structure and demographic history, as well as the processes and factors shaping them. Here, we investigated A . vaginata using ddRAD and whole-genome shotgun sequencing data from 138 individuals across 29 sampling localities spanning its distribution range. Integrated analyses of population genetic structure, demographic simulations, ecological niche simulation, phylogenomics, and ancestral range reconstruction were conducted to reconstruct the evolutionary history of this species. Our results identified four geographically structured lineages (southeast, northeast, northwest, and southwest), which were consistently supported by nuclear genomic analyses. Population genomics and demographic reconstruction indicated pronounced differences between northern and southern populations, with northern lineages exhibiting larger effective population sizes, higher genetic diversity, and more complex ancestral composition. These findings suggest that long-term geographic isolation, contrasting demographic histories, and heterogeneous landscape and climatic conditions have jointly shaped the present-day population genetic structure. Demographic simulations, phylogenomic reconstruction, ecological niche modeling and ancestral range reconstruction further support a demographic history consistent with a counterclockwise dispersal scenario around the HDM, in which historical climate oscillations and forest corridors may have facilitated dispersal around, rather than directly across the mountain system. Together, our results demonstrate that the four geographically structured lineages of A . vaginata were shaped by the interaction of historical demographic processes and environmental heterogeneity across its distribution range, providing new insights into the population history and phylogeographic evolution of A. vaginata .