Climatic Refugia and Geographical Isolation Contribute to the Speciation and Genetic Divergence in Himalayan-Hengduan Tree Peonies (Paeonia delavayi and Paeonia ludlowii)

Himalaya and Hengduan Mountains (HHM) is a biodiversity hotspot, and very rich in endemic species. Previous phylogeographical studies proposed different hypotheses (vicariance and climate-driven speciation) in explaining diversification and the observed pattern of extant biodiversity, but it is likely that taxa are forming in this area in species-specific ways. Here, we reexplored the phylogenetic relationship and tested the corresponding hypotheses within Paeonia subsect. Delavayanae composed of one widespread species (Paeonia delavayi) and the other geographically confined species (Paeonia ludlowii). We gathered genetic variation data at three chloroplast DNA fragments and one nuclear gene from 335 individuals of 34 populations sampled from HHM. We performed a combination of population genetic summary statistics, isolation-with-migration divergence models, isolation by environment, and demographic history analyses. We found evidence for the current taxonomic treatment that P. ludlowii and P. delavayi are two different species with significant genetic differentiation. The significant isolation by environment was revealed within all sampled populations but genetic distances only explained by geographical distances within P. delavayi populations. The results of population divergence models and demographic history analyses indicated a progenitor–derivative relationship and the Late Quaternary divergence without gene flow between them. The coalescence of all sampled cpDNA haplotypes could date to the Late Miocene, and P. delavayi populations probably underwent a severe bottleneck in population size during the last glacial period. Genetic variation in Paeonia subsect. Delavayanae is associated with geographical and environmental distances. These findings point to the importance of geological and climatic changes as causes of the speciation event and lineage diversification within Paeonia subsect. Delavayanae.