Lineage divergence and genome-wide genetic diversity in Fagus crenata : roles of mountain formation and climate oscillations

BACKGROUND AND AIMS: Understanding the evolutionary history of forest trees requires a broader temporal perspective extending beyond the last glacial maximum (LGM) to older geological, geomorphological and climatic processes. In Fagus crenata, a previous study revealed genetic divergence between populations on the Sea of Japan and Pacific sides of the Japanese Archipelago, but genome-wide patterns of genetic diversity and the demographic processes underlying lineage divergence remain unresolved. Using genome-wide SNPs, we investigated population genetic structure, geographic patterns of genetic diversity and historical population dynamics across the species' range. METHODS: We performed population genetic analyses using 2,097 genome-wide SNPs from 366 individuals representing 24 populations. For demographic inference, coalescent simulations were conducted under alternative divergence models using 147,638 SNPs. Species distribution modelling was used to reconstruct past potential habitats. KEY RESULTS: Genome-wide SNP analyses revealed a hierarchical population structure comprising one Sea of Japan-side lineage and two Pacific-side lineages. Genetic diversity tended to be lower in northern and southern populations than in central populations. Demographic inference indicated that the Sea of Japan-side and Pacific-side lineages diverged first, followed by divergence between the northeastern and southwestern Pacific-side lineages. Under the assumed generation time and mutation rate, these splits were estimated at circa (ca.) 2.46 Ma and 0.90 Ma, respectively, far predating the LGM. Migration rates were also estimated to have remained low until the late Quaternary, ca. 98 ka, and then increased, suggesting prolonged isolation followed by secondary contact. CONCLUSIONS: Lineage divergence and patterns of genome-wide genetic diversity in F. crenata may reflect not only late Quaternary range shifts but also older geological and climatic processes. Notably, mountain formation since the Late Pliocene, together with Quaternary climate oscillations, may have contributed to lineage divergence. These findings inform conservation-unit delineation and provide a basis for future studies of local adaptation in F. crenata.