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Late Pleistocene Speciation of Three Closely Related Tree Peonies Endemic to the Qinling–Daba Mountains, a Major Glacial Refugium in Central China

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Late Pleistocene Speciation of Three Closely Related Tree Peonies Endemic to the Qinling–Daba Mountains, a Major Glacial Refugium in Central China Received: 15 October 2018 | Revised: 22 April 2019 | Accepted: 8 May 2019 DOI: 10.1002/ece3.5284 ORIGINAL RESEARCH Late Pleistocene speciation of three closely related tree peonies endemic to the Qinling–Daba Mountains, a major glacial refugium in Central China Xing‐Xing Xu1 | Fang‐Yun Cheng1 | Li‐Ping Peng1 | Yan‐Qiang Sun2 | Xian‐Ge Hu2 | San‐Yuan Li3 | Hong‐Li Xian3 | Kai‐Hua Jia2 | Richard J. Abbott4 | Jian‐Feng Mao2 1Peony International Research Institute, National Flower Engineering Research Centre, Key Laboratory for the Genetics and Breeding of Forest Trees and Ornamental Plants, College of Landscape Architecture, Beijing Forestry University, Beijing, China 2Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, National Engineering Laboratory for Tree Breeding, Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, China 3Forestry Department of Shaanxi Province, Xi’an, Shaanxi, China 4School of Biology, Mitchell Building, University of St Andrews, St Andrews, Fife, UK Correspondence Fang‐Yun Cheng, Peony International Abstract Research Institute, National Flower Determining the factors promoting speciation is a major task in ecological and evo‐ Engineering Research Centre, Key Laboratory for the Genetics and Breeding of lutionary research and can be aided by phylogeographic analysis. The Qinling–Daba Forest Trees and Ornamental Plants, College Mountains (QDM) located in central China form an important geographic barrier be‐ of Landscape Architecture, Beijing Forestry University, Beijing, 100083, China. tween southern subtropical and northern temperate regions, and exhibit complex Email: [email protected] topography, climatic, and ecological diversity. Surprisingly, few phylogeographic anal‐ and Jian‐Feng Mao, Beijing Advanced Innovation yses and studies of plant speciation in this region have been conducted. To address Center for Tree Breeding by Molecular this issue, we investigated the genetic divergence and evolutionary histories of three Design, National Engineering Laboratory for Tree Breeding, Key Laboratory of closely related tree peony species (Paeonia qiui, P. jishanensis, and P. rockii) endemic to Genetics and Breeding in Forest Trees the QDM. Forty populations of the three tree peony species were genotyped using and Ornamental Plants, Ministry of Education; College of Biological Sciences 22 nuclear simple sequence repeat markers (nSSRs) and three chloroplast DNA se‐ and Technology, Beijing Forestry University, quences to assess genetic structure and phylogenetic relationships, supplemented by Beijing, 100083, China. Email: [email protected] morphological characterization and ecological niche modeling (ENM). Morphological and molecular genetic analyses showed the three species to be clearly differentiated Funding information the Natural Science Foundation of China, from each other. In addition, coalescent analyses using DIYABC conducted on nSSR Grant/Award Number: No. 31471898; the variation indicated that the species diverged from each other in the late Pleistocene, Key Technology Research of Oil Peony Industry in Shaanxi Province, Grant/Award while ecological niche modeling (ENM) suggested they occupied a larger area during Number: 2014HXFWYL016; Natural Science the Last Glacial Maximum (LGM) than at present. The combined genetic evidence Foundation of China, Grant/Award Number: 31471898 and 2014HXFWYL016; Special from nuclear and chloroplast DNA and the results of ENM indicate that each species project to Bulild World‐class Disciplines Of persisted through the late Pleistocene in multiple refugia in the Qinling, Daba, and Beijing Forestry University, Grant/Award Number: No. 2019XKJS0324 Taihang Mountains with divergence favored by restricted gene flow caused by geo‐ graphic isolation, ecological divergence, and limited pollen and seed dispersal. Our This is an open access article under the terms of the Creat ive Commo ns Attri bution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2019 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. Ecology and Evolution. 2019;00:1–21. www.ecolevol.org | 1 2 | XU ET AL. study contributes to a growing understanding of the origin and population structure of tree peonies and provides insights into the high level of plant endemism present in the Qinling–Daba Mountains of Central China. KEYWORDS ecological niche modeling, genetic divergence, multiple refugia, niche divergence, phylogeography, speciation, tree peony 1 | INTRODUCTION and ecological diversity, the Qinling–Daba Mountains provide an excel‐ lent setting for studying factors underlying divergence and speciation It is widely known that climatic fluctuations during the Pleistocene during the Pleistocene. Surprisingly, however, relatively few phylogeo‐ strongly impacted the distribution and genetic structure of plant and graphic studies of plants (Li, Wan, Guo, Abbott, & Rao, 2014; Shao & animal species in both Northern and Southern Hemispheres (Hewitt, Xiang, 2015; Yuan et al., 2012) compared to animals (Fang et al., 2015; 2004; Lu, Heckel, Liang, & Zhang, 2013; Song et al., 2009). Although Huang et al., 2017; Wang, Jiang, Xie, & Li, 2012, 2013; Yan, Wang, China experienced less severe glaciations during this period relative Chang, Xiang, & Zhou, 2010) have been conducted in this region. to Europe and North America (López‐Pujol, Zhang, Sun, Ying, & Ge, Tree peonies, which belong to section Moutan of the genus 2011; Qian & Ricklefs, 1999, 2000; Rost, 2000), climatic oscillations Paeonia (Hong & Pan, 2005; Stern, 1946), are distributed in central nonetheless affected the genetic diversity and evolution of many and northwestern China and include eight wild species (Hong, Pan, extant species in the region (Feng, Zheng, & Gong, 2016; Song et al., & Turland, 2001). Among them, four endemic species, Paeonia jis‐ 2009; Zhou et al., 2010). Recent phylogeographic surveys in China hanensis T. Hong & W. Z. Zhao, Paeonia rockii (S. G. Haw & Lauener), indicate that during Pleistocene glaciations montane species might T. Hong & J. J. Li, Paeonia qiui Y. L. Pei & D. Y. Hong, and Paeonia frequently have persisted in topographically complex regions that ostii T. Hong & J. X. Zhang, are mainly found in the Qinling–Daba served as refugia, rather than being restricted only to lower latitudes Mountains (Hong, 2010; Li, 2011), although P. ostii is listed as “criti‐ (Li et al., 2009; Liu et al., 2013; Qiu, Fu, & Comes, 2011; Song et al., cally Endangered” in the Threatened Species List of China's Higher 2009; Zhou et al., 2010). As one of the major areas of endemism in Plants (Qin et al., 2017) with extremely small populations owing to China (López‐Pujol et al., 2011), central China is characterized by a human overexploitation and domestication (Hong & Pan, 1999). Of complex topography with altitudes ranging from 100 to 3,767 m. The the remaining species, Paeonia rockii is widely distributed throughout relatively stable habitats within this region have enabled endemics a large part of the Qinling–Daba Mountains and extends northwards to persist and also provided conditions for new species to form in China at altitudes between 1,100 and 2,800 m, while Paeonia jis‐ throughout Quaternary oscillations (López‐Pujol et al., 2011; Ying, hanensis and P. qiui have more restricted distributions, being confined 1994; Ying & Zhang, 1993). However, in contrast to numerous phylo‐ to the northern and southern Qinling–Daba Mountains (Figure 1a), geographic surveys of plants from the Qinghai‐Tibet Plateau (Liu et respectively, at altitudes between 750 and 1,700 m (Hong et al., al., 2013; Luo et al., 2016; Zhang et al., 2018) and subtropical China 2001; Xu, Cheng, Xian, & Peng, 2016). (Fan et al., 2016; Wang et al., 2015) where the effects of climatic os‐ The three tree peony species are closely related showing minor cillations on genetic diversity have been well studied, relatively few morphological differences (Hong et al., 2001). Paeonia qiui has leaves phylogeographic analyses of plants in central China (Shao & Xiang, with nine leaflets that usually lack obvious purple‐red color above and 2015; Zhou et al., 2010) have been conducted, and consequently, is very similar to P. jishanensis, making their separate identification ex‐ little is currently known about mechanisms responsible for the high tremely difficult (Xu, Cheng, Peng, & Xian, 2017). Recent molecular phy‐ level of plant endemism found there. logenetic analysis has confirmed a close relationship among the three The Qinling–Daba Mountain range, located in central China, ex‐ species which are assigned to subsection Vaginatae (Zhang, Wang, Xia, tends east‐to‐west for nearly 2,500 km (Dong et al., 2011; Ying, 1994; & Zhou, 2009; Zhao, Zhou, Lin, Pan, & Li, 2008) with P. qiui and P. jis‐ Yuan, Cheng, & Zhou, 2012), forming an important geographical barrier hanensis considered as the most recently diverged sister species pair between China's northern temperate and southern subtropical regions, (Zhang et al., 2009; Zhao et al., 2008; Zhou et al., 2014). In phyloge‐ and representing a major watershed between the Yellow River and netic trees produced from chloroplast DNA sequences, placement of Yangtze River (Ma & He, 1988; Rost, 1994, 2000; Xia, 1990). During P. qiui/P. jishanensis and P. rockii indicates that introgression may have the Quaternary,
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