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Quaternary climate change and habitat preference shaped the genetic differentiation and phylogeography of Rhodiola sect. Prainia in the southern Qinghai-Tibetan Plateau.

ABSTRACT: There are two long-standing biogeographic hypotheses regarding the glacial survival of plant species in the Qinghai-Tibetan Plateau (QTP): the in situ survival hypothesis and the tabula rasa hypothesis. We tested these two hypotheses in a phylogeographic study of Rhodiola sect. Prainia, a monophyletic section with ecologically divergent lineages. Molecular data from the nuclear internal transcribed spacer, six plastid markers and 13 nuclear microsatellite loci were analyzed for 240 individuals from 19 populations of this section. Environmental data were used to analyze the niches of major phylogenetic lineages within this section and to model changes in their distributions since the Last Glacial Maximum (LGM). We found that Rhodiola sect. Prainia consists of three evolutionary lineages: all populations of R. stapfii, R. prainii populations at the southern edge of the QTP, and R. prainii populations in the interior part of the QTP. During the LGM, the survival of R. prainii in the interior part of the QTP corresponded with the in situ survival hypothesis, while R. stapfii most probably survived the LGM in a manner corresponding with the tabula rasa hypothesis. The evolutionary history of different lineages of this section was shaped by topography, climate change, and lineage-specific habitat preferences.

SUBMITTER: Wang ZM

PROVIDER: S-EPMC6662313 | biostudies-literature | 2019 Jul

REPOSITORIES: biostudies-literature

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Quaternary climate change and habitat preference shaped the genetic differentiation and phylogeography of Rhodiola sect. Prainia in the southern Qinghai-Tibetan Plateau.

Wang Zi-Meng ZM Meng Shi-Yong SY Rao Guang-Yuan GY

Ecology and evolution 20190630 14

There are two long-standing biogeographic hypotheses regarding the glacial survival of plant species in the Qinghai-Tibetan Plateau (QTP): the in situ survival hypothesis and the tabula rasa hypothesis. We tested these two hypotheses in a phylogeographic study of Rhodiola sect. Prainia, a monophyletic section with ecologically divergent lineages. Molecular data from the nuclear internal transcribed spacer, six plastid markers and 13 nuclear microsatellite loci were analyzed ...[more]

PMID: 31380091

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Project description:BackgroundAlthough allopatric speciation is viewed as the most common way in which species originate, allopatric divergence among a group of closely related species has rarely been examined at the population level through phylogeographic analysis. Here we report such a case study on eight putative cypress (Cupressus) species, which each have a mainly allopatric distribution in the Qinghai-Tibetan Plateau (QTP) and adjacent regions. The analysis involved sequencing three plastid DNA fragments (trnD-trnT, trnS-trnG and trnL-trnF) in 371 individuals sampled from populations at 66 localities.ResultsBoth phylogenetic and network analyses showed that most DNA haplotypes recovered or haplotype-clustered lineages resolved were largely species-specific. Across all species, significant phylogeographic structure (N(ST) > G(ST), P < 0.05) implied a high correlation between haplotypes/lineages and geographic distribution. Two species, C. duclouxiana and C. chengiana, which are distributed in the eastern QTP region, contained more haplotypes and higher diversity than five species with restricted distributions in the western highlands of the QTP. The remaining species, C. funebris, is widely cultivated and contained very little cpDNA diversity.ConclusionsIt is concluded that the formation of high mountain barriers separating deep valleys in the QTP and adjacent regions caused by various uplifts of the plateau since the early Miocene most likely promoted allopatric divergence in Cupressus by restricting gene flow and fixing local, species-specific haplotypes in geographically isolated populations. The low levels of intraspecific diversity present in most species might stem from population bottlenecks brought about by recurrent periods of unfavorable climate and more recently by the negative impacts of human activities on species' distributions. Our findings shed new light on the importance of geographical isolation caused by the uplift of the QTP on the development of high plant species diversity in the QTP biodiversity hotspot.

Project description:Aim:The evolutionary process of an organism provides valuable data toward an understanding of the Earth evolution history. To investigate the relationship between the uplift of the Qinghai-Tibet Plateau (QTP) and mammalian evolution since the late Cenozoic, the geographic distribution of genetic variations in the Tibetan hamster Cricetulus kamensis was investigated using phylogeographical methods. In particular, population divergence, demographic history, genetic variation, and the prediction of species distribution area were investigated. Location:The Qinghai-Tibet Plateau. Methods:A total of 53 specimens, representing 13 geographic populations, were collected from the QTP. The phylogeographical pattern and demographic history of C. kamensis were analyzed, and the probable factors in the QTP uplift and the Quaternary glacial periods were inferred from one nuclear and four mitochondrial genes. Furthermore, the species distribution model (SDM) was used to predict changes in potentially suitable habitats since the last Interglacial. Results:Phylogenetic analysis demonstrated that two major genetic differentiations of the C. kamensis population occurred during the Early Pleistocene that were influenced by the Qing-Zang tectonic movement from the Middle Pliocene to the Early Pleistocene. Genetic distance between two major clades indicated low genetic divergence. Demographic history analysis showed that the C. kamensis population was affected by the Quaternary glacial period. SDM analysis indicated that C. kamensis was endemic to the QTP and the suitable habitat was affected by climate change, especially during the Last Glacial Maximum (LGM). Main conclusion:Our results indicated that the QTP uplift led to the population divergence of C. kamensis, and vicariance well accounted for the geographic distribution of genetic variation in C. kamensis as a result of genetic divergence and lack of gene flow. The genetic distance shows that C. alticola may be a subspecies of C. kamensis. Demographic history analysis suggests that the QTP was affected by the last glacial period. SDM analysis supports that almost the entire QTP is covered by a huge ice sheet during the LGM.

Project description:The evolution and current distribution of the Sino-Tibetan flora have been greatly affected by historical geological events, such as the uplift of the Qinghai-Tibetan Plateau (QTP), and Quaternary climatic oscillations. Rhodiola kirilowii, a perennial herb with its distribution ranging from the southeastern QTP and the Hengduan Mountains (HM) to adjacent northern China and central Asia, provides an excellent model to examine and disentangle the effect of both geological orogeny and climatic oscillation on the evolutionary history of species with such distribution patterns. We here conducted a phylogeographic study using sequences of two chloroplast fragments (trnL-F and trnS-G) and internal transcribed spacers in 29 populations of R. kirilowii. A total of 25 plastid haplotypes and 12 ITS ribotypes were found. Molecular clock estimation revealed deep divergence between the central Asian populations and other populations from the HM and northern China; this split occurred ca. 2.84 million year ago. The majority of populations from the mountains of northern China were dominated by a single haplotype or ribotype, while populations of the HM harbored both high genetic diversity and high haplotype diversity. This distribution pattern indicates that HM was either a diversification center or a refugium for R. kirilowii during the Quaternary climatic oscillations. The present distribution of this species on mountains in northern China may have resulted from a rapid glacial population expansion from the HM. This expansion was confirmed by the mismatch distribution analysis and negative Tajima's D and Fu's FS values, and was dated to ca. 168 thousand years ago. High genetic diversity and population differentiation in both plastid and ITS sequences were revealed; these imply restricted gene flow between populations. A distinct isolation-by-distance pattern was suggested by the Mantel test. Our results show that in old lineages, populations may harbour divergent genetic forms that are sufficient to maintain or even increase overall genetic diversity despite fragmentation and low within-population variation.

Dataset Information

Quaternary climate change and habitat preference shaped the genetic differentiation and phylogeography of Rhodiola sect. Prainia in the southern Qinghai-Tibetan Plateau.

Publications

Quaternary climate change and habitat preference shaped the genetic differentiation and phylogeography of <i>Rhodiola</i> sect. <i>Prainia</i> in the southern Qinghai-Tibetan Plateau.

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