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Demographic Expansion of Loropetalum Chinense (Hamamelidaceae) in Chinese Subtropical Evergreen Broadleaved Forest

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Demographic Expansion of Loropetalum Chinense (Hamamelidaceae) in Chinese Subtropical Evergreen Broadleaved Forest Org Divers Evol DOI 10.1007/s13127-015-0252-4 ORIGINAL ARTICLE From glacial refugia to wide distribution range: demographic expansion of Loropetalum chinense (Hamamelidaceae) in Chinese subtropical evergreen broadleaved forest Wei Gong 1,2 & Wanzhen Liu 1 & Lei Gu1,3 & Shingo Kaneko 4 & Marcus A. Koch5 & Dianxiang Zhang1 Received: 1 July 2015 /Accepted: 19 November 2015 # Gesellschaft für Biologische Systematik 2015 Abstract The subtropical evergreen broadleaved forest combination with ecological niche modeling (ENM). ENM (STEBF) in China is globally one of the most diverse and indicated that the distribution ranges of L. chinense were biologically important forest systems. There has been a long- contracted remarkably and most populations retreated south- term debate whether this region was affected dramatically dur- ward. Thereby, based on ENM, geographical distribution pat- ing Pleistocene glaciation and deglaciation cycles, e.g., in terms tern of cpDNA haplotypes, and AFLP genetic clusters, one of range dimensions and changes in species richness. Here we glacial refuge was inferred in the Nanling Mountains in south- report a large-scale phylogeographic study, focusing on a wide- ern China, and a second glacial refuge was identified in Three spread and typical constituent species of the Chinese STEBF, Gorges Area and Dabashan Mountains in Chongqing Province, Loropetalum chinense (R. Br.) Oliver (Hamamelidaceae). In southwestern China. In addition to ENM, with mismatch dis- total, 56 populations spanning the entire distribution range of tribution analysis and Bayesian skyline plots, demographic ex- L. chinense were analyzed. Chloroplast DNA sequence varia- pansion was inferred to take place about 10.6 kya. The current tion and AFLPs as molecular marker systems were used in geographic distribution pattern of genetic variation might be shaped by northward and eastward expansion along Nanling Mountains and Wuyishan Mountains, respectively. Additional- Electronic supplementary material The online version of this article ly, the two mountain ranges were supposed to act as geograph- (doi:10.1007/s13127-015-0252-4) contains supplementary material, ical barriers restricting gene flow between the southern and which is available to authorized users. northern populations. Herewith, we aim to further contribute a case study of the phylogeographic history of this vegetation * Marcus A. Koch type, which will help to improve deeper understanding of past [email protected] vegetation dynamics and floristic evolutionary pathways of the * Dianxiang Zhang Chinese STEBF. [email protected] Keywords Widespread species . Phylogeography . 1 Key Laboratory of Plant Resources Conservation and Sustainable Postglacial history . Evergreen broadleaved forest Utilization, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou 510650, China 2 College of Life Sciences, South China Agricultural University, Guangzhou 510642, China Introduction 3 Peking University, Conservation Biology Building, Beijing 100871, China Climatic oscillations during the Quaternary glaciation and de- glaciation cycles have long been considered to have had pro- 4 Laboratory of Forest Biology, Division of Forest and Biomaterials Science, Graduate School of Agriculture, Kyoto University, found effects on the geographic distribution and spatial genet- Kyoto 606-8502, Japan ic pattern of extant species (Hewitt 2004). An overall “con- ” “ 5 Centre for Organismal Studies (COS) Heidelberg, Department of tract-expand model and genetic diversity pattern of southern Biodiversity and Plant Systematics, Heidelberg University, Im richness versus northern purity” have often been observed for Neuenheimer Feld 345, 69120 Heidelberg, Germany species occurring in European or northern American regions W. Gong et al. (Hewitt 2000). Accumulating evidence suggested that the ge- subtropical China was inferred to be a glacial refugium for netic structure of modern plant populations reflect aspects of T. wallichiana and Ginkgo biloba (Gao et al. 2007; Gong vegetational dynamics since at least the Last Glacial Maxi- et al. 2008). Additionally, the southwestern Dabashan Moun- mum (LGM: c. 21 kya), e.g., the locations of glacial refugia, tains, Daloushan Mountains, and the Sichuan Basin were in- trajectories of postglacial colonization and associated demo- ferred to be glacial refugia for Cathaya argyrophylla, graphic processes, as well as the aggregation and disaggrega- Cercidiphyllum japonicum, T. wallichiana, G. biloba,and tion of forest communities (Hewitt 2000; Petit et al. 2008;Hu E. cavaleriei (Wang and Ge 2006; Gao et al. 2007; Gong et al. 2009). Genetic evidence is now required to provide new et al. 2008;Wangetal.2009;Qietal.2012). Moreover, insights into past vegetational history and address important localized or fast range expansions from several and different paleoecological questions (Hu et al. 2009; McLachlan et al. refugia were detected in T. wallichiana, P. kwangtungensis, 2005;Shepherdetal.2007). Phylogeographic studies of wide- Quercus variabilis, Platycarya strobilacea, and Rhododen- spread species or constituent residents in a specific forest sys- dron simsii (Gao et al. 2007;Tianetal.2008, 2015;Chen tem have been especially important for interpreting the evolu- et al. 2012a, b;Lietal.2012;Xuetal.2014). Evidence for tionary history of species and their associated vegetation. eastward migration is also obtained in widespread species The subtropical evergreen broadleaved forest (STEBF) in such as F. longipetiolata (Liu 2008). China is one of the most important forest systems. It has out- The research presented here focused on Loropetalum standing plant richness and is one of the main biodiversity hot chinense (R. Br.) Oliver, an evergreen shrub or small tree, spots in Southeast Asia due to its large geographic and climat- belonging to the Hamamelidaceae family. It is one of the ic heterogeneity (Hou 1983; Wang 1992a, b; Myers et al. dominant residents of the STEBF with widespread distribu- 2000; Ying 2001). Several localized centers of plant diversity tion across the major mountain ranges in subtropical China. with high levels of endemism have been identified in topo- The most widely found populations of L. chinense display graphically diverse mountain ranges (Ying 2001). Simulated white flowers with terminal inflorescence. Two morphologi- vegetation maps have indicated that climatic cooling during cally variable populations were found with narrow distribu- the LGM caused southward shifts in the geographical distri- tions on the southern limit and exhibit either small white bution of all temperate vegetation species, being confined to flowers with axillary inflorescence or red flowers with termi- the most southern tropical part of China and forming a con- nal inflorescence. Previous studies revealed that seeds of tinuous vegetation band eastward to the Japanese archipelago L. chinense show ballistic dispersal model and fall down by via the East China Sea shelf (Harrison et al. 2001; Sun et al. gravity (Du et al. 2009). Pollination studies indicated self- 1999;Nietal.2010). The refugial populations of the STEBF compatibility of L. chinense; however, the possibility of expanded and advanced northward during the middle Holo- cross-pollination cannot be excluded as Thrips sp. has been cene (c. 6 kya) (Sun et al. 1999;Nietal.2010). Meanwhile, detected to exist inside the flowers (Gu and Zhang 2008;Gu evidence obtained from geographical data of the Quaternary 2008). Its congener Loropetalum subcordatum (Bentham) Ol- glaciation and deglaciation cycles has suggested an alternative iver, an endemic endangered species with contrastingly nar- hypothesis. No glaciers developed at low elevations below row and scattered distribution pattern in China, shows similar 2500 m in the eastern China mountainous regions (defined ecological preferences and is suggested to be autogamy based here as the subtropical region to the east of Qinghai-Tibet on previous studies (Gu and Zhang 2008;Gongetal.2010). Plateau) according to Shi et al. (2006) and Li et al. (2004), The third species in the genus, Loropetalum lanceum Hand.- but a cold and dry climate formed due to a strengthening Mzt., has not been recorded in recent decades and therefore winter monsoon (Shi et al. 2006). The effects of lower tem- was not included in the present study. The variety L. chinense perature and precipitation on subtropical region might also Oliver var. rubrum Yieh, which has red flowers and terminal cause the latitudinal and altitudinal migrations, population ex- inflorescence, was originally found in central China and is tinction, and range fragmentation and/or expansion. now cultivated widely. The increasing large-scale phylogeographic studies of plant Given the wide distribution of L. chinense in subtropical species in China supported multiple glacial refugia present in China and ballistic dispersal seeds by gravity, this species the widespread or component species in STEBF (Qiu et al. represents a good system to test if the STEBF component 2011)(Table1). The Hengduan Mountains and the Yungui plant species conform the Bcontract-expand^ model and assist Plateau in western China were identified as glacial refugia in a better understanding of the vegetative history of STEBF. for Taxus wallichiana, Fagus longipetiolata,andPinus Despite an increasing number of phylogeographic studies in kwangtungensis (Gao et al. 2007;Liu2008;Tianetal. China, few of them focus on the widespread or component 2010). The Nanling
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