Allopolyploid origin and niche expansion of Rhodiola integrifolia (Crassulaceae).

Polyploidy after hybridization between species can lead to immediate post-zygotic isolation, causing saltatory origin of new species. Although the incidence of polyploidization in plants is high, it is thought that a new polyploid lineage can succeed only if it establishes a new ecological niche divergent from its progenitor lineages. We tested the hypothesis that Rhodiola integrifolia from North America is an allopolyploid produced by R. rhodantha and R. rosea and determined whether its survival can be explained by the niche divergence hypothesis. To this end, we sequenced two low-copy nuclear genes (ncpGS and rpb2) in a phylogenetic analysis of 42 Rhodiola species and tested for niche equivalency and similarity using Schoener's D as the index of niche overlap. Our phylogeny-based approach showed that R. integrifolia possesses alleles from both R. rhodantha and R. rosea. Dating analysis showed that the hybridization event that led to R. integrifolia occurred ca. 1.67 Mya and niche modeling analysis showed that at this time, both R. rosea and R. rhodantha may have been present in Beringia, providing the opportunity for the hybridization event. We also found that the niche of R. integrifolia differs from that of its progenitors in both niche breadth and optimum. Taken together, these results confirm the hybrid origin of R. integrifolia and support the niche divergence hypothesis for this tetraploid species. Our results underscore the fact that lineages with no current overlapping distribution could produce hybrid descendants in the past, when climate oscillations made their distributions overlap.

Nunataks or massif de refuge? A phylogeographic study of Rhodiola crenulata (Crassulaceae) on the world's highest sky islands.

BACKGROUND: Quaternary climatic oscillations had tremendous effects on the current distribution of species. Here, we aim to elucidate the glacial history of Rhodiola crenulata, a perennial herb almost exclusively restricted to rock crevices on mountain peaks, and to test whether the nunatak or massif de refuge hypotheses could explain its distribution pattern. RESULTS: Six haplotypes and six ribotypes were detected in the cpDNA data set and the ITS data set, respectively. The divergence of R. crenulata and its closest relatives was dated have occurred ca. 0.65 Mya, during the Naynayxungla glaciation on the QTP. Mismatch distribution analysis suggested that the species experienced a range expansion around 0.31 Mya. Populations with high genetic and haplotype diversity were found on the QTP platform as well in the Hengduan Mountains. The ecological niche modeling results showed that there were suitable habitats on both the QTP platform and in the Hengduan Mountains during the LGM. CONCLUSION: Our results support a scenario that both nunataks and the massif de refuge hypotheses could explain the distribution of R. crenulata. We also confirmed that Quaternary climatic oscillations could promote plant speciation in some circumstances. This study adds to a growing body of evidence suggesting that the QTP plant lineages exhibited diverse reactions to the Quaternary climatic oscillations.

Climate Is Not All: Evidence From Phylogeography of Rhodiola fastigiata (Crassulaceae) and Comparison to Its Closest Relatives.

How geological events and climate oscillations in the Pleistocene glaciation shaped the geographic distribution of genetic variation of species on the Qinghai-Tibetan Plateau (QTP) and its adjacent areas has been extensively studied. However, little studies have investigated whether closely related species in the same genus with similar physiological and life history traits responded similarly to the glacial climatic oscillations. If this is not the case, we would expect that the population histories of studied species were not driven by extrinsic environmental changes alone. Here we conducted a phylogeographic study of a succulent alpine plant Rhodiola fastigiata, using sequences from chloroplast genome and nrITS region, as well as ecological niche modeling. The results of R. fastigiata were compared to other congeneric species that have been studied, especially to R. alsia and R. crenulata. We found that for both markers, two geographic groups could be revealed, corresponding to the QTP plateau and the Hengduan Mountains, respectively, indicating isolated refugia in those two areas. The two groups diverged 1.23 Mya during the Pleistocene. We detected no significant population expansion by mismatch distribution analysis and Bayesian Skyline Plot. We found that even these similar species with similar physiological and life history traits have had different demographic histories in the Quaternary glacial periods. Our comparative phylogeographic study sheds new lights into phylogeographic research that extrinsic environmental changes are not the only factor that can drive population demography, and other factors, such as coevolved interactions between plants and their specialized pathogens, that probably played a role need to be examined with more case studies.

Author Correction: Establishment of the most comprehensive ITS2 barcode database to date of the traditional medicinal plant Rhodiola (Crassulaceae).

A correction to this article has been published and is linked from the HTML and PDF versions of this paper. The error has been fixed in the paper.

Gone with the trees: Phylogeography of Rhodiola sect. Trifida (Crassulaceae) reveals multiple refugia on the Qinghai-Tibetan Plateau.

Quaternary climatic oscillations have had tremendous effects on current distribution of species. Previous studies unraveled multiple microrefugia on the Qinghai-Tibetan Plateau (QTP) in two woody plants. Still we know little whether herbs growing in forests responded to climatic oscillations similarly. We herein conducted a phylogeographic study on Rhodiola sect. Trifida, an herbaceous group endemic to the QTP, which mainly growing on the forest floors, using plastid and ITS sequences as well as ecological niche modeling. The origin and divergence of major clades of sect. Trifida were in accordance with the last phase of the QTP uplifts. Mismatch distribution analysis indicated a range expansion dated to ca. 135 thousand years ago. A high frequency and an even distribution of private haplotypes in both plastid and ITS data sets throughout the distribution of sect. Trifida were detected. The ecological niche modeling results showed that there were suitable habitats on the QTP platform during the LGM. Our results found that multiple microrefugia existed on the QTP platform, supporting the hypothesis that species with similar geographic distribution and inhabiting the same community had similar responses to the Quaternary climatic oscillations. Furthermore, species delimitations in sect. Trifida need to be tested based on integrative evidence from morphological, ecological and genetic data.

Establishment of the most comprehensive ITS2 barcode database to date of the traditional medicinal plant Rhodiola (Crassulacaee).

The roots and rhizomes of Rhodiola crenulata and R. rosea have been used worldwide as adaptogens for hundreds of years. However, rapid growth in demand has resulted in merchants using other species of Rhodiola as adulterants. Here, we surveyed 518 individuals representing 47 of the 55 species in the genus, including 253 R. crenulata individuals from 16 populations and 98 R. rosea individuals from 11 populations, to evaluate the utility of the internal transcribed spacer 2 (ITS2) barcode for identification of Rhodiola species. We detected six haplotypes in R. crenulata and only one haplotype in R. rosea. An obvious overlap between intra- and inter-specific distance was detected, and the authentication efficacy of ITS2, which was assessed by BLAST1, a nearest distance method, and a tree test, was much lower than in other groups. However, R. crenulata and R. rosea could be exactly identified. Analysis showed that the secondary structure of ITS2 differs in R. crenulata and its closest relatives. Our results demonstrated that both a mini barcode from ITS2 and the structure of ITS2 are effective markers for the identification of R. crenulata and R. rosea. This study represents the most comprehensive database of ITS2 barcodes in Rhodiola to date and will be useful in Rhodiola species identification.