Eomecon Chionantha

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Eomecon Chionantha Tian et al. BMC Evolutionary Biology (2018) 18:20 DOI 10.1186/s12862-017-1093-x RESEARCH ARTICLE Open Access Phylogeography of Eomecon chionantha in subtropical China: the dual roles of the Nanling Mountains as a glacial refugium and a dispersal corridor Shuang Tian1,2†, Yixuan Kou1†, Zhirong Zhang3†, Lin Yuan1, Derong Li1, Jordi López-Pujol4, Dengmei Fan1* and Zhiyong Zhang1* Abstract Background: Mountains have not only provided refuge for species, but also offered dispersal corridors during the Neogene and Quaternary global climate changes. Compared with a plethora of studies on the refuge role of China’s mountain ranges, their dispersal corridor role has received little attention in plant phylogeographic studies. Using phylogeographic data of Eomecon chionantha Hance (Papaveraceae), this study explicitly tested whether the Nanling Mountains, which spans from west to east for more than 1000 km in subtropical China, could have functioned as a dispersal corridor during the late Quaternary in addition to a glacial refugium. Results: Our analyses revealed a range-wide lack of phylogeographic structure in E. chionantha across three kinds of molecular markers [two chloroplast intergenic spacers, nuclear ribosomal internal transcribed spacer (nrITS), and six nuclear microsatellite loci]. Demographic inferences based on chloroplast and nrITS sequences indicated that E. chionantha could have experienced a strong postglacial range expansion between 6000 and 1000 years ago. Species distribution modelling showed that the Nanling Mountains and the eastern Yungui Plateau were the glacial refugia of E. chionantha. Reconstruction of dispersal corridors indicated that the Nanling Mountains also have acted as a corridor of population connectivity for E. chionantha during the late Quaternary. Conclusions: Our results suggest that the Nanling Mountains may acted dual roles as a dispersal corridor in east-west direction and as a glacial refugium in subtropical China during the late Quaternary. The population connectivity mediated by the mountain range and a strong postglacial range expansion are the most likely reasons for the lack of phylogeographic structure in E. chionantha. The hypothesis of dual roles of the mountain range presented here sheds new insights into the phylogeographic patterns of organisms in subtropical China. Keywords: Phylogeographic structure, Chloroplast intergenic spacer, Ribosomal internal transcribed spacer, Microsatellite, Dispersal corridor, Eomecon chionantha Hance * Correspondence: [email protected]; [email protected]; [email protected] †Equal contributors 1Laboratory of Subtropical Biodiversity, Jiangxi Agricultural University, Nanchang, Jiangxi 330045, China Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Tian et al. BMC Evolutionary Biology (2018) 18:20 Page 2 of 12 Background Tertiary lineages (such as Cathaya, Ginkgo, Glyptostrobus, Given their extremely diverse topography and a wide Metasequoia, and so forth) that were once widely distrib- spectrum of environmental conditions within short dis- uted along the Northern Hemisphere are today endemic tances, mountains have generally provided refuge for to China [9, 10]. An important reason is that a high per- species, especially during the Neogene and Quaternary centage of the mountainous lands in the country (in China global climate changes [1–3].Inaddition,mountains over 50% is mountainous [11]) served as refuge areas for have often offered dispersal corridors, allowing for range those ancient lineages [2, 10, 12–15]. During the past expansions/contractions, population connection, and gene decade, increasing molecular phylogeographic studies flow between otherwise fragmented populations [1, 4, 5]. on Chinese plant species showed that climatic refugia Both functions of refuge and dispersal corridor are ex- identified by DNA-based data (reviewed in [16, 17]) are tremely important for the persistence of organisms during largely congruent with the centers of endemism [15], periods of large climate change such as the late Cenzoic highlighting the sheltering function of China’smoun- [6]. For example, many mid-elevation mountain ranges tain ranges. However, compared with numerous studies and hilly areas in southern and central Europe did not ontherefugeroleofChina’s mountain ranges, their only provide shelters for the survival of Fagus sylvatica function as dispersal corridors has received much less during the Quaternary glacial periods, but also facilitate attention (but see [18, 19]). In addition, the mountain cor- the northward spread of the residual populations during ridors in China have been mostly inferred subjectively ac- inter−/postglacial periods, because beeches found their cording to the distribution patterns of certain taxa or humid habitats that were absent on the great plains [7]. genetic lineages, while very few have been tested explicitly Such cases were also reported in the Korean Peninsula using reproducible methods (but see [20]). of east Asia. The uninterrupted Baekdudaegan Moun- The Nanling Mountains sensu lato (i.e., including the tains, that runs from north to south over 1600 km, mountains on the Guangxi-Guangdong and Hunan-Jiangxi acted as a true dispersal corridor for a large assemblage borders) is a series of five connected mountain ranges that of boreal and temperate elements during the Quater- spans from west to east for more than 1000 km (Fig. 1c): nary climate changes beyond serving as a refugium for Yuechengling, Dupangling, Mengzhuling, Qitianling and many species [5]. Dayuling mountains. Also known as the “Five Mountains”, Harboring more than 30,000 vascular plants, China is and though not very high (average about 1000 m), the one of 17 world’s megadiversity countries [8]. Many Nanling range is a natural dividing line in subtropical Fig. 1 a Distribution of chloroplast haplotypes of Eomecon chionantha. b The network of 15 chloroplast haplotypes. c The distribution of Eomecon chionantha in China, the Nanling mountains is indicated with dark red color Tian et al. BMC Evolutionary Biology (2018) 18:20 Page 3 of 12 China, effectively separating the Yangtze (Changjiang) rhizomes to form patches, sampled individuals were River drainage area (characterized by a central or north- spaced by ca. 20–50 m to avoid repeatedly collecting subtropical climate) from the Pearl (Zhujiang) River drain- the same individual (i.e., ramets belonging to the same age area (of south-subtropical or tropical climate). The genet) except for a few small populations. All samples Nanling Mountains is one of the key biodiversity hotspots were desiccated in silica gel and stored at −20 °C until in China [14, 21] and has long been viewed as a major gla- being processed. Genomic DNA was extracted using a cial refugium [12, 16, 17] as well as an important ‘ice-free’ modified CTAB procedure [27]. corridor in east-west direction [16, 18]. While its role as a Two intergenic spacers (IGSs) of the chloroplast genome, glacial refugium has been demonstrated by different rbcL-atpB[28]andtrnC-rpoB [29], and nuclear ribosomal studies, robust evidence for the role of a corridor is still internal transcribed spacer (nrITS)[30]wereamplifiedand lacking. sequenced. The PCR primers of the three genomic frag- Eomecon chionantha Hance is a perennial herb (10– ments are listed in Additional file 1. Amplification reactions 30 cm in height) of the monotypic genus Eomecon from were carried out in a volume of 20 μl, containing 10 μl2× the poppy family (Papaveraceae, [22]). The Chinese name Taq PCR MasterMix (Tiangen, Shanghai, China), 1 μl each xueshuicao means ‘bleeding herb’ because its leaves and forward and reverse primer (0.2 uM), 1 μltemplateDNA rhizomes ooze orange-red sap when bruised or cut. It is (ca. 50–100 ng) and 7 μlddH2O. Amplification was carried an entomophilous species (with bees and flies being the out in a Bioer XP cycler (Bioer, Hangzhou, China) pro- mostefficientpollinators)thathasmixed-matingsys- grammed for an initial step of 240 s at 94 °C, followed by tem [23]. E. chionantha is a rhizomatous plant that also 30 cycles of 60 s at 94 °C, 60 s at 50 °C (rbcL-atpB), 50 °C produces subterranean runners, which allows vegetative (trnC-rpoB),or53°C(nrITS),60sat72°C,andafinal propagation. It is a potentially important economic plant step of 600 s at 72 °C. Sequencing reactions were con- given the molluscicidal activity of its alkaloids (they have ducted with the corresponding forward and reverse shown to be active against Oncomelania hupensis,the primers commercially by Sangon Biotech Co., Ltd. only intermediate host of Schistosoma japonicum in (Shanghai, China). Six nuclear microsatellite (or nuclear China; [24]). E. chionantha always grows in shady and simple sequence repeat, nSSR) loci (XSCO35, XSCO37, moisthabitatsalongstreamsortrailsinforestsorat XSCO78, XSCQ13, XSCQ25, XSCQ60) that were spe- forest margins in mountainous areas (300–2000 m; [22]).
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