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Phylogeny of the Paleotropical Fern Genus Lepisorus (Polypodiaceae, Polypodiopsida) Inferred from Four Chloroplast DNA Regions

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Phylogeny of the Paleotropical Fern Genus Lepisorus (Polypodiaceae, Polypodiopsida) Inferred from Four Chloroplast DNA Regions Molecular Phylogenetics and Evolution 54 (2010) 211–225 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Phylogeny of the paleotropical fern genus Lepisorus (Polypodiaceae, Polypodiopsida) inferred from four chloroplast DNA regions Li Wang a,b,c,d, Xin-ping Qi a,d, Qiao-ping Xiang a, Jochen Heinrichs b, Harald Schneider b,c,*, Xian-chun Zhang a,* a State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, The Chinese Academy of Sciences, Beijing 100093, China b Albrecht-von-Haller Institute of Plant Sciences, Georg-August University Göttingen, Untere Karspüle 2, 37073 Göttingen, Germany c Department of Botany, The Natural History Museum London, London SW7 5BD, UK d Graduate University of Chinese Academy of Sciences, Beijing 100049, China article info abstract Article history: Phylogenetic relationships within the paleotropical genus Lepisorus (Polypodiaceae) were investigated Received 4 April 2009 using plastid DNA sequences from four regions: rbcL, rps4 and rps4-trnS IGS, trnL intron plus trnL-F IGS, Revised 24 August 2009 rbcL-atpB IGS. Over 4000 nucleotides were sequenced for 77 specimens belonging to 54 species. Each Accepted 25 August 2009 cpDNA region was analyzed separately and combined into a single dataset. All phylogenetic analyses, Available online 6 September 2009 maximum parsimony, maximum likelihood and Bayesian Inference of phylogeny, revealed the paraphyly of Lepisorus with the monotypic Drymotaenium miyoshianum and of the paleotropical genus Belvisia Keywords: nested within the Lepisorus clade. Nine well-supported major clades were found. The phylogenetic results Molecular phylogeny provided new evidence for the sectional classification of Lepisorus. The evolution of three morphological Lepisorus Drymotaenium characters, clathrateness of rhizome scales, margin of rhizome scales and defoliated leaves, and the evo- Belvisia lution of the karyotype, were reconstructed to identify lineage specific phenotypic character states or Platygyria combination of characters. Unique character combinations, rather than synapomorphies, were found to Morphological character evolution be of systematic value in sectional delimitation. The variation of chromosome numbers is largely due Chromosome numbers to a single aneuploidy event instead of a stepwise reduction during the evolutionary history of this genus. Cytology Ó 2009 Elsevier Inc. All rights reserved. 1. Introduction nized already the group as a distinct entity. Ching (1933) pointed out remarkable difference from the Neotropical genus Pleopeltis The fern genus Lepisorus (J. Sm.) Ching comprises about 40 Humb. and Bonpl. ex Willd., with which Lepisorus was frequently species according to some researchers (Hennipman et al., 1990; confused in the past. Despite of many voices of disapproval Zink, 1993), but more than 68 are recognized alone from China (Copeland, 1947; Pichi-Sermolli, 1977), many Asian pteridologists (Lin, 2000). The genus is distributed throughout the Old World accepted Lepisorus as a distinct genus. At the end of the 20th cen- tropics and subtropics with a diversity center in the Sino-Hima- tury, many pteridologists approved Ching’s classification layan region, the proposed area of origin (Zink, 1993), and a sec- (Hennipman et al., 1990; Zink, 1993) and finally phylogenetic stud- ond smaller diversity center in the Afromadagascan region (Zink, ies based on DNA sequence data proved the distant relationship 1993). The genus Lepisorus is commonly found in tropical to between Lepisorus and Pleopeltis (Schneider et al., 2004b,c). temperate areas of eastern Asia, with a few species extending Although there is strong support for the independent generic sta- to the Malaysian region including New Guinea and with one spe- tus, relationships among Lepisorus and supposedly affine species are cies reaching the Hawaiian Islands. Lepisorus members are com- thus far inconclusive. Ching and Wu (1980) segregated a putative mon epiphytes or lithophytes (Zink, 1993), from very low genus Platygyria Ching from Lepisorus and Hennipman et al. (1990) altitudes in eastern Asia up to 5000 m in the arid Himalayas. assigned Paragramma (Blume) T. Moore to be a synonym of Lepisorus. Some species of Lepisorus even have medicinal properties (Abla Recently, molecular phylogenetic results revealed that Belvisia Mir- and Ababakri, 2007). bel and Drymotaenium Makino were embedded within Lepisorus Based on morphological distinctness, Ching (1933) raised Lepis- (Kreier et al., 2008; Schneider et al., 2004c). These analyses indicated orus to generic rank for the first time, although Smith (1846) recog- Lepisorus to be paraphyletic and demonstrated the need of an exhaustive study on the intrageneric and intergeneric relationships. At a local scale, Zink (1993) published a comprehensive revi- * Corresponding authors. sion of Afromadascan Lepisorus, in which nine species were rec- E-mail addresses: [email protected], [email protected] (H. ognized. Whereafter, Yu and Lin (1996, 1997) made a Schneider), [email protected] (X.-c. Zhang). 1055-7903/$ - see front matter Ó 2009 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2009.08.032 212 L. Wang et al. / Molecular Phylogenetics and Evolution 54 (2010) 211–225 comprehensive revision of Chinese species and delimited six extensive sampling, we intend to: (1) reconstruct the phylogeny sections (Lepisorus, Pleioomma S.L. Yu, Sclerophyllon S.L. Yu, of the genus Lepisorus, (2) explore the relationships of Lepisorus Macrophyllon S.L. Yu, Pachyphyllon S.L. Yu and Hymenophyton and its affinities such as Belvisia, Drymotaenium and Platygyria, Ching ex. S.L. Yu and Y.X. Lin). Finally, Lin (2000) modified this (3) evaluate the evolution of selected morphological characters, classification in the context of Flora of China, in which only and (4) to explore the evolution of the karyotype. The last question two sections (Lepisorus and Hymenophyton) were kept. Recently, is of particular interest because Lovis (1977) mentioned this genus Liu et al. (2008) made a taxonomic revision of section Hymeno- to be of great significance in relation to our understanding of cyto- phyton, in which they reduced the number of accepted species logical evolution of ferns. from 16 to 5. However, up to the present, neither a taxonomic revision nor a molecular phylogeny focused on Lepisorus on a worldwide scale has been released. 2. Materials and methods Species delimitation and intrageneric classification within Lepisorus has been subject of controversial discussion, because 2.1. Taxonomic sampling many of the taxonomically informative characters reflect quantita- tive rather than qualitative variation. In addition, characters used Our taxon sampling was designed in consideration of the results to differentiate species show variation within some species. The of previous morphology-based studies (Ching, 1978a,b; Ching intrageneric classification is often founded on the shape and struc- et al., 1983; Hovenkamp, 1998; Lin, 2000; Liu et al., 2008; Yu ture of the rhizome scales and paraphyses (Lin, 2000; Liu et al., and Lin, 1996, 1997; Zhang et al., 2003; Zink, 1993) and DNA-based 2008; Yu and Lin, 1996; Zink, 1993). Rhizome scales are always studies (Kreier et al., 2008; Schneider et al., 2004c). We took spe- considered to be the most important character for the classification cial attention to represent all sections proposed by Yu and Lin of Lepisorus: shape of rhizome scales varies from lanceolate (1997) and to include all morphologically distinct putative lineages (Fig. 1F), ovate-lanceolate (Fig. 1D) to ovate-orbicular; most spe- within this genus. We sampled also carefully the three genera cies own completely clathrate rhizome scales (Fig. 1D and E), and found to be nested within Lepisorus as well as the sometimes-ac- a small number of species exhibit partly clathrate rhizome scales cepted segregate genus Paragramma. In total 70 individuals, (Fig. 1A and B) and completely non-clathrate rhizome scales respectively, 54 species of Lepisorus, including representatives of (Fig. 1C); margins of rhizome scales are also variable in different all sections of Lepisorus, were sampled to obtain a comprehensive species, entire (Fig. 1D) or toothed (Fig. 1E). taxonomic coverage of the paleotropical fern genus Lepisorus. The Given the morphological uniformity of the genus, molecular sampling included 54 species out of about 70 species currently data are required to depict phylogenetic relationships among these known for Lepisorus and represented all currently recognized sec- species. However, Lepisorus has received scant phylogenetic atten- tions (Lin, 2000; Yu and Lin, 1997). In addition, five representatives tion. To date, the best sampling of Lepisorus can be ascribed to from the genera Belvisia, Drymotaenium and Paragramma were also Kreier et al.’s study (2008), even in which only a few species were included since they were most closely related to Lepisorus (Kreier included. The study, however, recovered evidence for the para- et al., 2008; Schneider et al., 2004c). Multiple DNA accessions from phyly of Lepisorus in respect to Belvisia, Drymotaenium and Platygy- different distributional regions were sampled for some species that ria. To address the question of the monophyly of Lepisorus, we need are taxonomically difficult to circumscribe. Four species represent- a more comprehensive taxon sampling, which is provided in this ing the genera Lemmaphyllum C. Presl, Neocheiropteris Christ,
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