Abstract
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.
Highlights
Mountains are often hotspots of endemism, where the geological activities and climatic changes are historically frequent, driving lineage divergence, and speciation both in tropical and temperate regions (Myers et al, 2000; Perrigo et al, 2020)
P. delavayi were collected from 31 locations covered the geographic distribution range (YP: Yunnan Plateau, HDM: Hengduan Mountains, and EH: East Himalaya) and three populations of P. ludlowii were sampled to represent the geographical spread in Mainling, Tibet (EH) (Supplementary Table 1)
The cpDNA alignment consisted of 335 sequences of 2,500 bp yielding 33 haplotypes defined by 35 nucleotide substitutions, 26 indels, and one inversion within the combined three fragments (Supplementary Table 3)
Summary
Mountains are often hotspots of endemism, where the geological activities and climatic changes are historically frequent, driving lineage divergence, and speciation both in tropical and temperate regions (Myers et al, 2000; Perrigo et al, 2020). Climatic factors are often as dynamic as topography, and climatic changes over space and time may promote speciation via niche conservatism or niche divergence (Hua and Wiens, 2013). If allopatric speciation associated with geographical isolation was the dominant mode of lineage differentiation or speciation, we would expect most sister–species pairs to be allopatrically distributed, but they might show little ecological niche differentiation because this would not be needed for speciation to occur, and new species tends to keep the ancestor niche (i.e., niche conservatism; Wiens and Graham, 2005). Comparatively little is known about the potential role of ecological factors in the process of species or lineage diversification, and ecology-driven genetic divergence has seldom been examined (Meng et al, 2015; Zhao et al, 2016; Gao et al, 2019)
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