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A Preliminary Species-Level Phylogeny of the Alpine Ginger Roscoea: Implications for Speciation

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A Preliminary Species-Level Phylogeny of the Alpine Ginger Roscoea: Implications for Speciation Journal of Systematics JSE and Evolution doi: 10.1111/jse.12247 Research Article A preliminary species-level phylogeny of the alpine ginger Roscoea: Implications for speciation Jian-Li Zhao1,2, Jinshun Zhong3, Yong-Li Fan2,4, Yong-Mei Xia2, and Qing-Jun Li1* 1Laboratory of Ecology and Evolutionary Biology, State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan University, Kunming 650091, China 2Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Mengla 666303, China 3Department of Plant Biology, University of Vermont, 63 Carrigan Drive, Burlington, VT 05405, USA 4China Forest Exploration and Design Institute of Kunming, Kunming 650216, China *Author for correspondence. E-mail: [email protected]. Tel.: 86-871-65030660. Received 13 December 2016; Accepted 1 March 2017; Article first published online xx Month 2017 Abstract Speciation, the evolutionary process forming new species, is a key mode generating biodiversity on the Earth. In this study, we produced a species-level phylogeny of Roscoea using one nuclear ribosomal and two chloroplast DNA fragments based on Bayesian inference and maximum likelihood. We then explored the possible speciation processes using the species-level phylogeny and the heterozygous sites in the nuclear DNA. The incongruence between nuclear and chloroplast phylogenies, and several heterozygous sites in the nuclear DNA, suggested that R. auriculata might have a hybrid origin with R. purpurea and R. alpina being two possible parental progenitors; however, one alternative possibility through incomplete lineage sorting cannot be ruled out. In addition, R. kunmingensis likely originated from R. tibetica Batalin through the process of “budding speciation”. These results provided a valuable framework to draw testable hypotheses for future in-depth comparative studies to further our understanding of the underpinning speciation and adaptation mechanisms that contribute to ultrahigh biodiversity in the Himalayas and the Hengduan Mountains. Key words: biodiversity hotspots, budding speciation, hybridization, phylogenetics, Roscoea. 1 Introduction taxonomic treatment (Wu & Kai, 2000; Cowley, 2007; Luo et al., 2007; Mao & Bhaumik, 2007). Roscoea species are Speciation, the formation of new species through splitting, unique in that many adapt to high-elevation regions (>4000 m hybridization, or polyploidization, is a key evolutionary process above sea level), for instance, R. alpina Royle in the HIM and R. that produces biodiversity on Earth (Coyne & Orr, 2004; Butlin tibetica Batalin in the Hengduan Mountains, whereas the rest et al., 2009). Exploring the patterns of speciation in a biological of the Zingiberaceae family occur mostly in pantropics and group through phylogenetic reconstruction can provide insight subtropics (Kress et al., 2002; Cowley, 2007). Field observation into the origin of biodiversity, especially in biodiversity hotspots and molecular studies have suggested that Roscoea showed (e.g., Richardson et al., 2001a, 2001b; Liu et al., 2006; Che et al., disjunct distribution between the Himalayas and the Heng- 2010; Zhao et al., 2016b). With diverse and rich endemic species, duan Mountains in northern Indochina (NIC) (Ngamriabsakul the Himalayas (HIM) and the Hengduan Mountains are et al., 2000; Cowley, 2007) (Fig. 1). A recent study also revealed considered two such hotspots (Myers et al., 2000; Mutke & that the origin and disjunction of Roscoea was associated with Barthlott, 2005). Many genus-level phylogenies have been the uplift of the Himalayan–Tibetan Plateau and the rapid inferred to assess the patterns and origins of high biodiversity extrusion of Indochina, respectively, with Roscoea in NIC likely in these two regions, such as the vicariance of warblers being derived from those in HIM (Zhao et al., 2016b). Thus, the (Johansson et al., 2007), Paini (Che et al., 2010), and Roscoea genus Roscoea is an ideal group in which to assess the Smith (Zhao et al., 2016b), and radiation of Isodon (Schrad. ex speciation patterns and processes underlying their radiation in Benth.) Spach (Yu et al., 2014) and Abies Mill. (Peng et al., 2015). these two biodiversity hotspots. However, in-depth species-level speciation study of the Previous phylogenies of Roscoea were poorly supported endemic genera is still lacking. Thus, more detailed intrageneric due to limited taxonomic sampling and insufficient phyloge- phylogenies, especially for the endemic genera, are critically netic signals using only a single molecular marker (Ngamriab- needed to uncover the general and/or unique speciation sakul et al., 2000). Although dense population-level sampling fi processes during alpine species diversi cation. strategy in a phylogeographic study has provided compelling The genus Roscoea Smith (Zingiberaceae) is endemic to the evidence for the disjunction of Roscoea between the HIM and Sino-HIM, including 22 species according to the latest NIC (Zhao et al., 2016b), reticulate evolution caused by recent XXX 2017 | Volume 9999 | Issue 9999 | 1–10 © 2017 Institute of Botany, Chinese Academy of Sciences 2 Zhao et al. Fig. 1. Sampling of Roscoea species along the Himalayas (HIM) and Hengduan Mountains of northern Indochina (NIC). gene flow and introgression after speciation may be too Sang et al., 1995; Techaprasan et al., 2006). Polymerase chain noisy to infer species-level phylogeny, despite diverse distinct reaction (PCR) was carried out in a total volume of 50 mL morphologies among species (Fig. 2). Therefore, extended reaction including 1Â PCR buffer (50 mmol/L KCl, 10 mmol/L phylogenetic analyses for Roscoea with broader species-level Tris, pH 8.0), 2 mmol/L MgCl2, 0.2 mmol/L dNTP, 1 mmol/L sampling and additional molecular markers are needed. In this primer, 0.25 U Taq DNA polymerase, and approximately 10 ng study, we inferred phylogenies of Roscoea using nuclear genomic DNA template. We used the following PCR internal transcribed spacers (nrITS) and chloroplast DNA conditions: 94 °C for 5 min, followed by 35 cycles of (cpDNA). We then used these results to assess species 94 °C for 30 s, annealing temperatures for 30 s and 72 °C for relationships and proposed hypotheses of likely speciation 1.5 min, with a final extension at 72 °C for 15 min. The annealing modes for future in-depth speciation analyses. temperatures were 56 °C, 53 °C, and 56 °C for nrITS, psbA-trnH, and trnL-F, respectively. The PCR products were bidirectionally sequenced using the amplification primers on an ABI 3730 2 Material and Methods DNA Analyzer (Applied Biosystems, Foster City, CA, USA). If unreadable peak signals or conflict were found between 2.1 Taxon sampling and DNA sequencing bidirectional sequences at the same locus for one individual, Morphological species concept of Roscoea (sensus Wu & Kai, sequences were re-amplified and resequenced to ensure 2000; Cowley, 2007) was used for field sampling. Forty-eight that heterozygous sites (double peaks) were not the artifacts accessions representing 18 of 22 total delimited Roscoea of sequencing error. DNA sequences of H. gardnerianum species were collected from the HIM and NIC (Fig. 1). The were obtained from GenBank (nrITS, AY424759; psbA-trnH, remaining four species are distributed in a very small, KC597931; trnL-F, AY424787). The newly generated sequences restricted area and were not sampled in this study, including of Roscoea and Cautleya have been submitted to the GenBank R. ganeshensis Cowley & W.J. Baker, R. brandisii (King ex database with accession numbers KY210313–KY210363 (nrITS), Baker) K. Schum., R. ngainoi A.A. Mao & Bhaumik, and R. KY210364–KY210414 (psbA-trnH), and KY210415–KY210465 cangshanensis M.H. Luo, X.F. Gao & H.H. Lin (Table 1). We used (trnL-F). Cautleya J.D. Hooker (C. gracilis (Sm.) Dandy and C. spicata (Sm.) Baker) and Hedychium gardnerianum Roscoe as out- groups according to previous studies (Kress et al., 2002; Zhao 2.2 Phylogenetic reconstruction et al., 2016b). Sequences were aligned using MAFFT (Katoh et al., 2002) Total genomic DNA from silica-dried leaves for each followed by manual adjustment in MEGA version 5 (Tamura accession was extracted using the CTAB protocol (Doyle & et al., 2011). Chloroplast psbA-trnH and trnL-F were Doyle, 1987). We used ITS1-5.8S–ITS2 nrITS and cpDNA psbA- concatenated for phylogenetic inference. Gaps were coded trnH, including the partial trnH gene, and trnL-F, including the using the sample-coding method (Simmons & Ochoterena, partial trnF gene using previous primers (Taberlet et al., 1991; 2000) in SeqState version 1.4.1 (Muller,€ 2005). We ran the J. Syst. Evol. 9999 (9999): 1–10, 2017 www.jse.ac.cn Species-level phylogeny of Roscoea 3 Fig. 2. Diverse species of Roscoea (A–L) and phylogram of the 50% major consensus tree (M,N). A, R. tibetica Batalin. B, R. kunmingensis. C, R. debilis. D, R. cautleoides. E, R. humeana. F, R. schneideriana. G, R. alpina. H, R. bhutanica. I, R. auriculata. J, R. purpurea. K, R. tumjensis. L, R. capitata. Bayesian inference and maximum likelihood analyses of nuclear internal transcribed spacer (M) and chloroplast DNA (N). The topology of the phylogram is a best Bayesian inference tree. Bayesian posterior probability and maximum likelihood bootstrap support values are listed above and below the corresponding branches, respectively. Asterisks show that support values are higher than 90%; oblique lines show that support values are lower than 50%. Thick lines indicate species with heterozygous sites. Numbers following the species are the sample identifiers. Double slash indicates branch is shortened. Cautleya (C. gracilis and C. spicata)andHedychium gardnerianum are the outgroups. HIM, Himalayan; NIC, northern Indochina. www.jse.ac.cn J. Syst. Evol. 9999 (9999): 1–10, 2017 4 Zhao et al. Table 1 Sampling and vouchers of Roscoea Sm. and Cautleya Hook. f † Species Sample ID Location Specimen code R. alpina Royle 64301 Thyangsyapu, Nepal XYM643 70006 Yadong, Xizang, China HITBC150257 R. auriculata K. Schum. 75101 Nagahot, Nepal XYM751 75102 Nagahot, Nepal XYM751 R. bhutanica Ngamr. 69901 Yadong, Xizang, China HITBC150256 R. capitata Sm. 63701 Bamboo, Nepal XYM637 76002 Ricemphet, Nepal XYM760 77101 Tumje, Nepal XYM771 77601 Charikot, Nepal XYM776 R.
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