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A Global Plastid Phylogeny of the Brake Fern Genus Pteris (Pteridaceae) and Related Genera in the Pteridoideae

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A Global Plastid Phylogeny of the Brake Fern Genus Pteris (Pteridaceae) and Related Genera in the Pteridoideae Cladistics Cladistics (2014) 1–18 10.1111/cla.12094 A global plastid phylogeny of the brake fern genus Pteris (Pteridaceae) and related genera in the Pteridoideae Liang Zhanga, Carl J. Rothfelsb, Atsushi Ebiharac, Eric Schuettpelzd, Timothee Le Pechona, Peris Kamaue, Hai Hef, Xin-Mao Zhoua, Jefferson Pradog, Ashley Fieldh,i, George Yatskievychj, Xin-Fen Gaoa,* and Li-Bing Zhangj,* aChengdu Institute of Biology, Chinese Academy of Sciences, P.O. Box 416, Chengdu, Sichuan, 610041, China; bDepartment of Zoology, University of British Columbia, #4200-6270 University Blvd., Vancouver, BC, V6T 1Z4, Canada; cDepartment of Botany, National Museum of Nature and Science, Tsukuba-shi, Ibaraki, 305-0005, Japan; dDepartment of Botany (MRC 166), National Museum of Natural History, Smithsonian Institution, P.O. Box 37012, Washington, DC, 20013-7012, USA; eDepartment of Botany, National Museum of Kenya, P.O. Box 45166-00100, Nairobi, Kenya; fDepartment of Biology, Chongqing Normal University, Shapingba, Chongqing, 400047, China; gInstituto de Botanica^ Herbario SP, Avenida Miguel Estefano 3687, CEP 04301-012, Sao~ Paulo, Brazil; hAustralian Tropical Herbarium, James Cook University, Smithfield, Qld, 4878, Australia; iQueensland Herbarium, Department of Science, Information Technology, Innovation and the Arts, Toowong, Qld, 4066, Australia; jMissouri Botanical Garden, P.O. Box 299, St Louis, MO, 63166-0299, USA Accepted 30 June 2014 Abstract The brake fern genus Pteris belongs to the Pteridaceae subfamily Pteridoideae. It contains 200–250 species distributed on all continents except Antarctica, with its highest species diversity in tropical and subtropical regions. The monophyly of Pteris has long been in question because of its great morphological diversity and because of the controversial relationships of the Austra- lian endemic monospecific genus Platyzoma. The circumscription of the Pteridoideae has likewise been uncertain. Previous stud- ies typically had sparse sampling of Pteris species and related genera and used limited DNA sequence data. In the present study, DNA sequences of six plastid loci of 146 accessions representing 119 species of Pteris (including the type of the genus) and 18 related genera were used to infer a phylogeny using maximum-likelihood, Bayesian-inference and maximum-parsimony methods. Our major results include: (i) the previous uncertain relationships of Platyzoma were due to long-branch attraction; (ii) Afropter- is, Neurocallis, Ochropteris and Platyzoma are all embedded within a well-supported Pteris sensu lato; (iii) the traditionally cir- cumscribed Jamesonia is paraphyletic in relation to a monophyletic Eriosorus; (iv) Pteridoideae contains 15 genera: Actiniopteris, Anogramma, Austrogramme, Cerosora, Cosentinia, Eriosorus, Jamesonia, Nephopteris (no molecular data), Onychium, Pityrogram- ma, Pteris, Pterozonium, Syngramma, Taenitis and Tryonia; and (v) 15 well-supported clades within Pteris are identified, which differ from one another on molecular, morphological and geographical grounds, and represent 15 major evolutionary lineages. © The Willi Hennig Society 2014. Introduction one of the largest fern genera, Pteris has been estimated to contain ca. 200 (Tryon and Tryon, The fern genus Pteris L. (Pteridaceae: Pteridoideae; 1982) or 250 species (Tryon et al., 1990) distributed Tryon et al., 1990) is characterized by having sporan- throughout the tropical, subtropical, and temperate gia borne continuously along most of the length of areas of all continents except Antarctica, from the pinnae from commissural veins, and having Australia, New Zealand and South Africa northward pinnae that are entire or pectinately divided into to Japan and North America. From open slopes to segments (with these sometimes asymmetrical). As dense forests and from acid soils to limestone rock, the habitats of Pteris are diverse, and the genus *Corresponding authors: includes considerable morphological variation (Liao E-mail addresses: [email protected]; [email protected] et al., 2013). © The Willi Hennig Society 2014 2 L. Zhang et al. / Cladistics (2014) 1–18 The circumscription of Pteris has been unstable 2004b; Prado et al., 2007; Schuettpelz et al., 2007; since its establishment by Linnaeus (1753). A broad Bouma et al., 2010; Schneider et al., 2013; Cochran concept of the genus initially included most ferns with et al., 2014), or three or four (Schuettpelz et al., 2007; continuous sori along pinna margins, even those now Cochran et al., 2014) plastid genes, there have been recognized to fall in other families (e.g. Pteridium very few studies focusing on the relationships within Gled. ex Scop.). Some later concepts, relying heavily Pteris. Li et al. (2004) used trnL-F intergenic spacer on venation patterns (Presl, 1836; Moore, 1857), were sequences (< 400 base pairs) from 16 Chinese species very narrow and placed most species in segregated to reconstruct the first phylogeny of Pteris, and con- genera (e.g. Campteria C. Presl and Litobrochia C. cluded that Pteris was strongly supported as mono- Presl). Since the twentieth century, it has generally phyletic and that P. vittata L. was resolved as the been agreed that: (i) species of Doryopteris J. Sm., His- earliest diverging lineage. However, Platyzoma R. Br. tiopteris (J. Agardh) J. Sm., Paesia J. St.-Hil. and was not sampled and only one distantly related out- Pteridium should be excluded from Pteris; (ii) the gen- group, Adiantum capillus-veneris L., was included in eric recognition of Campteria,“Eupteris” and Litobro- their analysis. Using rbcL gene sequences of 10 species chia should be abandoned; and (iii) the names of Pteris and related genera in Pteridaceae, Prado corresponding to the distinct venation patterns should et al. (2007) found that Pteris was paraphyletic in rela- be used for infrageneric classification. tion to Platyzoma, a monospecific Australian endemic. In comparison with the instability of the definition of Based on atpA, atpB and rbcL gene data from nine Pteris, the infrageneric relationships of Pteris are far species of Pteris and a broad sampling of related gen- clearer (Presl, 1836; Smith, 1841; Moore, 1857; Hooker era, Schuettpelz et al. (2007) discovered that Pteris and Baker, 1868). The latest global classification of was also paraphyletic with respect to Neurocallis Fee Pteris is that published by Christensen (1906). Based on (a Neotropical monospecific genus), Ochropteris J. Sm. different venation patterns, three existing sections, (a Malagasy and Mascarene bispecific genus), and “P. sect. Eupteris” (nom. inval. = P. sect. Pteris), Platyzoma. Most interestingly, Schuettpelz et al. (2007) P. sect. Heterophlebium (Fee) Hook. and P. sect. Lito- found that P. vittata, a species morphologically similar brochia (C. Presl) Hook. were accepted, and later three to the type of the genus (P. longifolia L., not sampled subgenera “P. subg. Eupteris”(= P. subg. Pteris), in their study), was not resolved as closely allied to the P. subg. Campteria (C. Presl) C. Chr., and P. subg. remainder of the genus. They suggested that the defini- Litobrochia (C. Presl) C. Chr., were proposed. In spite tion of Pteris would need to be expanded to include of the obvious artificiality of Christensen’s (1906) infra- their entire “pteridoid clade” (Rothfels, 2008) or generic classification (Walker, 1962), many more recent reduced to the small clade of P. longifolia, P. vittata taxonomic studies have adopted it to a large extent (e.g. and their close allies. More recent studies of the Pte- Wu, 1990; Yang, 2011; Liao et al., 2013). The earliest ridaceae (e.g. Bouma et al., 2010; Chao et al., 2012a; competitor to Christensen’s system was that of Shieh Jaruwattanaphan et al., 2013; Schneider et al., 2013) (1966), who emphasized the importance of patterns of have provided only limited information concerning the leaf architecture and proposed a reclassification into phylogeny of Pteris. To date, there have not been any two subgenera, P. subg. Pteris (leaves pinnate or bipin- large-scale multilocus molecular phylogenetic studies nate) and P. subg. Tripedipteris W. C. Shieh (leaves of Pteris. tripartite), with the two subgenera each divided into Pteris is normally placed in the subfamily Pteridoi- two sections: P. subg. Pteris into P. sect. Pteris and deae. The circumscription of the latter, however, has P. sect. Campteria (C. Presl) Hook., and P. subg. Trip- been controversial: Tryon et al. (1990) placed five edipteris into P. sect. Hypsopodium W. C. Shieh and genera in the Pteridoideae and 13 genera in the P. sect. Tripedipteris W. C. Shieh. Combining the pat- Taenitidoideae; Sanchez-Baracaldo (2004b) rejected terns of frond architecture and venation type, Tryon the monophyly of the Taenitidoideae sensu Tryon and Tryon (1982) divided the Neotropical species of et al. (1990) using rps4-trnS data; Smith et al. (2006) Pteris into six unranked groups. Finally, in classifying combined the two subfamilies; Schuettpelz et al. (2007) species of Pteris of China, Ching and Wu (1983) recog- suggested that the Taenitidoideae lineage was nested nized three sections, P. sect. Pteris, P. sect. Campteria within the Pteridoideae. The sampling of taxa and/or and P. sect. Quadriauricula Ching, with the last two characters so far has been limited. each further divided into two series. Ching and Wu’s The objectives of this study were: (i) to resolve the classification was adopted in a recent taxonomic treat- relationships within the Pteridoideae; (ii) to test the ment in Flora of China (Liao et al., 2013). monophyly
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