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A Large-Scale Phylogeny of the Lycophyte Genus Selaginella (Selaginellaceae: Lycopodiopsida) Based on Plastid and Nuclear Loci

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A Large-Scale Phylogeny of the Lycophyte Genus Selaginella (Selaginellaceae: Lycopodiopsida) Based on Plastid and Nuclear Loci See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/281275639 A large-scale phylogeny of the lycophyte genus Selaginella (Selaginellaceae: Lycopodiopsida) based on plastid and nuclear loci ARTICLE in CLADISTICS · AUGUST 2015 Impact Factor: 6.22 · DOI: 10.1111/cla.12136 CITATION READS 1 362 12 AUTHORS, INCLUDING: Carl J Rothfels Ngan Lu University of California, Berkeley Vietnam Academy of Science and Technology 37 PUBLICATIONS 539 CITATIONS 10 PUBLICATIONS 12 CITATIONS SEE PROFILE SEE PROFILE Ralf Knapp David Lorence Independent Researcher National Tropical Botanical Garden 4 PUBLICATIONS 4 CITATIONS 102 PUBLICATIONS 961 CITATIONS SEE PROFILE SEE PROFILE All in-text references underlined in blue are linked to publications on ResearchGate, Available from: Li-Bing Zhang letting you access and read them immediately. Retrieved on: 28 January 2016 Cladistics Cladistics (2015) 1–30 10.1111/cla.12136 A large-scale phylogeny of the lycophyte genus Selaginella (Selaginellaceae: Lycopodiopsida) based on plastid and nuclear loci Xin-Mao Zhoua,b, Carl J. Rothfelsc,d, Liang Zhanga, Zhao-Rong Hee, Timothee Le Pechona,f, Hai Heg, Ngan Thi Luh, Ralf Knappi, David Lorencej, Xing-Jin Heb, Xin-Fen Gaoa,* and Li-Bing Zhangk,* aChengdu Institute of Biology, Chinese Academy of Sciences, PO Box 416, Chengdu, Sichuan 610041, China; bSchool of Life Sciences, Sichuan University, Chengdu, Sichuan 610064, China; cDepartment of Zoology, University of British Columbia, #4200-6270 University Blvd, Vancouver, BC V6T 1Z4, Canada; dUniversity Herbarium and Department of Integrative Biology, University of California, Berkeley, CA 94720-2465, USA; eSchool of Life Science, Yunnan University, Kunming, Yunnan 650091, China; fSchool of Life Sciences, University of KwaZulu-Natal, Private Bag X01 Scottsville, Pietermaritzburg 3209, South Africa; gDepartment of Biology, Chongqing Normal University, Shapingba, Chongqing 400047, China; hDepartment of Botany, Vietnam National Museum of Nature, Vietnam Academy of Science and Technology, 18th Hoang Quoc Viet Road, Cau Giay, Ha Noi, Viet Nam; iCorrespondent of the Museum national d’Histoire naturelle (MNHN, Paris, France), Steigestrasse 78, 69412 Eberbach, Germany; jNational Tropical Botanical Garden, 3530 Papalina Road, Kalaheo, HI 96741, USA; kMissouri Botanical Garden, PO Box 299, St Louis, MO 63166-0299, USA Accepted 28 June 2015 Abstract The lycophyte genus Selaginella alone constitutes the family Selaginellaceae, the largest of the lycophyte families. The genus is estimated to contain 700–800 species distributed on all continents except Antarctica, with highest species diversity in tropical and subtropical regions. The monophyly of Selaginella in this broad sense has rarely been doubted, whereas its intrageneric clas- sification has been notoriously contentious. Previous molecular studies were based on very sparse sampling of Selaginella (up to 62 species) and often used DNA sequence data from one genome. In the present study, DNA sequences of one plastid (rbcL) and one nuclear (ITS) locus from 394 accessions representing approximately 200 species of Selaginella worldwide were used to infer a phylogeny using maximum likelihood, Bayesian inference and maximum parsimony methods. The study identifies strongly supported major clades and well resolves relationships among them. Major results include: (i) six deep-level clades are discovered representing the deep splits of Selaginella; and (ii) 20 major clades representing 20 major evolutionary lineages are identified, which differ from one another in molecular, macro-morphological, ecological and spore features, and/or geographical distribution. © The Willi Hennig Society 2015. The lycophyte family Selaginellaceae contains only climbing, creeping, prostrate and special rosetting one genus, Selaginella P. Beauv. The largest lycophyte forms. Many species of Selaginella are medicinally genus, Selaginella is cosmopolitan and is estimated to important and are reported as sources of bioactive com- contain 700 (Tryon and Lugardon, 1991), 750 (Jermy, pounds (Banks, 2009; Setyawan, 2011; da Silva Almeida 1990) or ca. 800 species (X.-M. Zhou and L.-B. Zhang, et al., 2013). Recently, the nuclear genome of one spe- unpublished data), which inhabit an impressive range of cies of the genus, Selaginella moellendorffii Hieron., has habitats, including desert, tropical rain forest, and been sequenced. This makes the genus enormously alpine and arctic habitats. Members of the genus also important in studying the evolution of vascular plants, have highly diverse growth forms, including erect, as the species is the only seed-free vascular plant whose nuclear genome is known so far (Banks et al., 2011; *Corresponding authors: Sessa et al., 2014). E-mail addresses: [email protected]; [email protected] © The Willi Hennig Society 2015 2 Xin-Mao Zhou et al. / Cladistics 0 (2015) 1–30 Selaginella was established by Palisot-Beauvois (1804) tional genera in the family. Rothmaler (1944) divided based on S. selaginoides (L.) P. Beauv. ex Mart. & Selaginella into three genera: Didiclis P. Beauv., Schrank. The genus was characterized by usually having Lycopodioides Boehm. and Selaginella sensu stricto (s.s.). distinct-sized and dorsiventral leaves in four rows, pre- The last two were accepted by some later authors (e.g. senting a ligule at the base of each leaf and sporophyll, Kung, 1988; Sojak, 1993; Tzvelev, 2004). Sojak (1993) and having heterospores (microspores and megaspores) and Weakley (2012) instead recognized Selaginella, and rhizophores (Thomas, 1997). Before Spring’s (1850) Lycopodiodes and Bryodesma Sojak in the family. major monograph of the genus, Selaginella was usually Based on plastid rbcL sequences of 18 species of Se- treated as a synonym of another lycophyte genus, Ly- laginella, Korall et al. (1999) conducted the first copodium L. (Lycopodiaceae) (e.g. Greville and Hooker, molecular analysis of the family, and recovered the 1831). Although the delimitation of Selaginella has monophyly of the genus and S. subg. Selaginella,and rarely been controversial [but see Rothmaler’s (1944), resolved the latter as sister to the rest of species sam- Sojak’s (1993), Kung’s (1988) and Tzvelev’s (2004) clas- pled. Later Korall and Kenrick (2002) increased the sifications below], the intrageneric classification within taxon sampling to 62 species and found support for Selaginella has been notoriously contentious (Spring, the monophyly of “S. subg. Tetragonostachys” too, 1850; Braun, 1857; Hieronymus and Sadebeck, 1901; and identified a so-called “dorsal rhizophoric” clade Walton and Alston, 1938; Rothmaler, 1944; Tryon and that included all species having a distinctive and Tryon, 1982; Jermy, 1986, 1990; Kung, 1988), with taxo- unique root-like structure (the rhizophore) emerging nomic treatments differing dramatically in the number from dorsal surfaces. This later study further discov- of subgenera/sections recognized. In general, previous ered the polyphyly of S. subg. Stachygynandrum and authors tended to divide Selaginella into two primary S. subg. Heterostachys, but their analysis was uncer- subdivisions, including the isophyllous versus aniso- tain about the monophyly of S. subg. Ericetorum. phyllous species, respectively. For example, Spring Using nuclear 26S and rbcL data of 23 species, Korall (1840) divided the genus into three sections: S. sect. Se- and Kenrick (2004) resolved the dorsal rhizophoric laginella (autonym, implied), S. sect. Homoeophyllae clade into two major subclades, although neither of Spring and S. sect. Heterophyllae Spring and similarly which is characterized by a clear morphological Braun (1857) also recognized three sections but named synapomorphy. Most recently, based on nuclear ITS them S. sect. Selaginella, S. sect. Dichotropae (internal transcribed spacer) and rbcL data of 40 A. Braun and S. sect. Homotropae A. Braun, while mainly North American species, Arrigo et al. (2013) Moore (1857) instead used S. sect. Diplostachyum confirmed the monophyly of “S. subg. Tetragonos- (P. Beauv.) T. Moore and S. sect. Stachygynandrum (P. tachys” and resolved it as sister to S. lepidophylla Beauv. ex Mirb.) T. Moore for the latter two. Hierony- (Hook. & Grev.) Spring, a species native to the Chi- mus and Sadebeck (1901) also recognized two groups, huahuan Desert of the USA and Mexico and known but at the rank of subgenus: S. subg. Homoeophyllum for its ability to survive almost complete desiccation. Hieron. & Sadeb. and S. subg. Heterophyllum Hieron. Arrigo et al. (2013) showed that the “dorsal rhi- & Sadeb. Based on morphology (especially that of stro- zophoric’’ clade defined by Korall and Kenrick (2002) bili) and habit forms, Warburg (1900), Walton and is paraphyletic or polyphyletic. Alston (1938) and Jermy (1986, 1990) subdivided the Notably, previous molecular studies focused mainly genus further. Warburg (1900) recognized five subgen- on the two species-poor subgenera only, Selaginella era in the genus: S. subg. Boreoselaginella Warb., subg. Selaginella (2 spp.) and “S. subg. Tetragonos- “S. subg. Euselaginella” (nom. inval., = S. subg. tachys” (ca. 50 spp.), while S. subg. Heterostachys and Selaginella), S. subg. Heterostachys Baker, S. subg. S. subg. Stachygynandrum, which contain a total of Homostachys Baker and S. subg. Stachygynandrum (P. ca. 660 species (Tryon and Lugardon, 1991), were Beauv. ex Mirb.) Baker. Walton and Alston (1938) weakly sampled yet nonetheless were resolved as poly- accepted Warburg’s (1900)
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