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Recurrent hybridization underlies the evolution of novelty in Gentiana (Gentianaceae) in the Qinghai-Tibetan Plateau.

ABSTRACT: The Qinghai-Tibetan Plateau (QTP) and adjacent areas are centres of diversity for several alpine groups. Although it is known that the QTP acted as a source area for diversification of the alpine genus Gentiana, the evolutionary processes underlying diversity in this genus, especially the formation of narrow endemics, are still poorly understood. Hybridization has been proposed as a driver of plant endemism in the QTP but few cases have been documented with genetic data. Here, we describe a new endemic species in Gentiana section Cruciata as G. hoae sp. nov., and explore its evolutionary history with complete plastid genomes and nuclear ribosomal internal transcribed spacer sequence data. Genetic divergence within G. hoae ~3 million years ago was followed by postglacial expansion on the QTP, suggesting Pleistocene glaciations as a key factor shaping the population history of G. hoae. Furthermore, a mismatch between plastid and nuclear data suggest that G. hoae participated in historical hybridization, while population sequencing show this species continues to hybridize with the co-occurring congener G. straminea in three locations. Our results indicate that hybridization may be a common process in the evolution of Gentiana and may be widespread among recently diverged taxa of the QTP.

SUBMITTER: Fu PC

PROVIDER: S-EPMC7821390 | biostudies-literature | 2021 Feb

REPOSITORIES: biostudies-literature

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Recurrent hybridization underlies the evolution of novelty in <i>Gentiana</i> (Gentianaceae) in the Qinghai-Tibetan Plateau.

Fu Peng-Cheng PC Twyford Alex D AD Sun Shan-Shan SS Wang Hong-Yu HY Xia Ming-Ze MZ Tan Cheng-Xi CX Zhou Xiao-Jun XJ Chen Shi-Long SL

AoB PLANTS 20201202 1

The Qinghai-Tibetan Plateau (QTP) and adjacent areas are centres of diversity for several alpine groups. Although it is known that the QTP acted as a source area for diversification of the alpine genus <i>Gentiana</i>, the evolutionary processes underlying diversity in this genus, especially the formation of narrow endemics, are still poorly understood. Hybridization has been proposed as a driver of plant endemism in the QTP but few cases have been documented with genetic data. Here, we describe ...[more]

PMID: 33510891

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Project description:Background and aimsHosting several global biodiversity hotspots, the region of the Qinghai-Tibetan Plateau (QTP) is exceptionally species-rich and harbours a remarkable level of endemism. Yet, despite a growing number of studies, factors fostering divergence, speciation and ultimately diversity remain poorly understood for QTP alpine plants. This is particularly the case for the role of hybridization. Here, we explored the evolutionary history of three closely related Gentiana endemic species, and tested whether our results supported the mountain geo-biodiversity hypothesis (MGH).MethodsWe genotyped 69 populations across the QTP with one chloroplast marker and 12 nuclear microsatellite loci. We performed phylogeographical analysis, Bayesian clustering, approximate Bayesian computation and principal components analysis to explore their genetic relationship and evolutionary history. In addition, we modelled their distribution under different climates.Key resultsEach species was composed of two geographically distinct clades, corresponding to the south-eastern and north-western parts of their distribution. Thus Gentiana veitchiorum and G. lawrencei var. farreri, which diverged recently, appear to have shared at least refugia in the past, from which their range expanded later on. Indeed, climatic niche modelling showed that both species went through continuous expansion from the Last Interglacial Maximum to the present day. Moreover, we have evidence of hybridization in the northwest clade of G. lawrencei var. farreri, which probably occurred in the refugium located on the plateau platform. Furthermore, phylogenetic and population genetic analyses suggested that G. dolichocalyx should be a geographically limited distinct species with low genetic differentiation from G. lawrencei var. farreri.ConclusionsClimatic fluctuations in the region of the QTP have played an important role in shaping the current genetic structure of G. lawrencei var. farreri and G. veitchiorum. We argue that a species pump effect did occur prior to the Last Interglacial Maximum, thus lending support to the MGH. However, our results do depart from expectations as suggested in the MGH for more recent distribution range and hybridization dynamics.

Project description:BackgroundThe genus Swertia is of great medicinal importance and one of the most taxonomically challenging taxa within Gentianaceae, largely due to the morphological similarities of species within this genus and with its closely related genera. Previous molecular studies confirmed its polyphyly but suffered from low phylogenetic resolutions because only limited sequence loci were used. Thus, we conducted the structural, gene evolutionary, and phylogenetic analyses of 11 newly obtained plastomes of Swertia. Our result greatly improved the phylogenetic resolutions in Swertia, shed new light on the plastome evolution and phylogenetic relationships of this genus.ResultsThe 11 Swertia plastomes together with the published seven species proved highly similar in overall size, structure, gene order, and content, but revealed some structural variations caused by the expansion and contraction of the IRb region into the LSC region, due to the heterogeneous length of the ψycf1. The gene rps16 was found to be in a state flux with pseudogenes or completely lost. Similar situation was also documented in other genera of Gentianaceae. This might imply loss of the gene in the common ancestor of Gentianaceae. The distribution plot of ENC vs. GC3 showed all these plastomes arranging very close in the Wright line with an expected ENC value (49-52%), suggesting the codon usage of Swertia was mainly constrained by a GC mutation bias. Most of the genes remained under the purifying selection, however, the cemA was identified under positive selection, possibly reflecting an adaptive response to low CO2 atmospheric conditions during the Late Miocene. Our phylogenomic analyses, based on 74 protein-coding genes (CDS), supported the polyphyly of Swertia with its close allies in the subtribe Swertiinae, presumably due to recent rapid radiation. The topology inferred from our phylogenetic analyses partly supported the current taxonomic treatment. Finally, several highly variable loci were identified, which can be used in future phylogenetic studies and accurate identification of medicinal genuineness of Swertia.ConclusionsOur study confirmed the polyphyly of Swertia and demonstrated the power of plastome phylogenomics in improvement of phylogenetic resolution, thus contributing to a better understanding of the evolutionary history of Swertia.

Dataset Information

Recurrent hybridization underlies the evolution of novelty in Gentiana (Gentianaceae) in the Qinghai-Tibetan Plateau.

Publications

Recurrent hybridization underlies the evolution of novelty in <i>Gentiana</i> (Gentianaceae) in the Qinghai-Tibetan Plateau.

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