A global plastid phylogeny of the brake fern genus Pteris (Pteridaceae) and related genera in the Pteridoideae

Peris Kamau

The present paper deals with classification of extant Pteridophytes on the basis of their morphological features after brief reviewing of various systems of classification of the Pteridophytes. Accordingly, the authors planned to make the systematics of Pteridophytes easier and proposed the present classification with new concept including the following skeletal categorization i.e. division, class, subclass, order and family. The present proposal of Pteridophyte classification is the incorporation of all the species of extant Pteridophytes into 04 divisions, 06 classes, 13 subclass, 22 orders and 29 families. Lycopodiophyta divided in 01 class and 03 subclass, orders, families. Equisetophyta and Psilotophyta have single class, subclass, order and family. Filicophyta divided in 03 classes, 08 subclasses, 17 orders and 24 families. Accordingly, this is new approach for resolving the taxonomic problem amongst taxonomists throughout the world.

The Neotropical fern genera Eriosorus and Jamesonia have long been thought of as close relatives. Molecular phylogenetic studies have confirmed this notion but have also revealed that neither genus is monophyletic with respect to the other. As a result, all known species of Eriosorus were recently subsumed under the older generic name Jamesonia. Here, through an analysis of a four-gene plastid dataset, we show that several species traditionally treated in Eriosorus are in fact more closely related to other taenitidoid fern genera (namely Austrogramme, Pterozonium, Syngramma, and Taenitis) than they are to the large Jamesonia sensu lato clade. Tryonia Schuettp., J.Prado & A.T.Cochran gen. nov. is described to accommodate these species and four new combinations are provided. Tryonia is confined to southeastern Brazil and adjacent Uruguay; it is distinct (from most species of Jamesonia) in having stramineous rachises.

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,* a Chengdu 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 Bot^ anica Herb ario SP, Avenida Miguel Est efano 3687, CEP 04301-012, S~ ao 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; j Missouri 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 Australian endemic monospecific genus Platyzoma. The circumscription of the Pteridoideae has likewise been uncertain. Previous studies 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) Afropteris, Neurocallis, Ochropteris and Platyzoma are all embedded within a well-supported Pteris sensu lato; (iii) the traditionally circumscribed 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, Pityrogramma, 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 The fern genus Pteris L. (Pteridaceae: Pteridoideae; Tryon et al., 1990) is characterized by having sporangia borne continuously along most of the length of the pinnae from commissural veins, and having pinnae that are entire or pectinately divided into segments (with these sometimes asymmetrical). As *Corresponding authors: E-mail addresses: xfgao@cib.ac.cn; Libing.Zhang@mobot.org © The Willi Hennig Society 2014 one of the largest fern genera, Pteris has been estimated to contain ca. 200 (Tryon and Tryon, 1982) or 250 species (Tryon et al., 1990) distributed throughout the tropical, subtropical, and temperate areas of all continents except Antarctica, from Australia, New Zealand and South Africa northward to Japan and North America. From open slopes to dense forests and from acid soils to limestone rock, the habitats of Pteris are diverse, and the genus includes considerable morphological variation (Liao et al., 2013). 2 L. Zhang et al. / Cladistics (2014) 1–18 The circumscription of Pteris has been unstable since its establishment by Linnaeus (1753). A broad concept of the genus initially included most ferns with continuous sori along pinna margins, even those now recognized to fall in other families (e.g. Pteridium Gled. ex Scop.). Some later concepts, relying heavily on venation patterns (Presl, 1836; Moore, 1857), were very narrow and placed most species in segregated genera (e.g. Campteria C. Presl and Litobrochia C. Presl). Since the twentieth century, it has generally been agreed that: (i) species of Doryopteris J. Sm., Histiopteris (J. Agardh) J. Sm., Paesia J. St.-Hil. and Pteridium should be excluded from Pteris; (ii) the generic recognition of Campteria, “Eupteris” and Litobrochia should be abandoned; and (iii) the names corresponding to the distinct venation patterns should be used for infrageneric classification. In comparison with the instability of the definition of Pteris, the infrageneric relationships of Pteris are far clearer (Presl, 1836; Smith, 1841; Moore, 1857; Hooker and Baker, 1868). The latest global classification of Pteris is that published by Christensen (1906). Based on different venation patterns, three existing sections, “P. sect. Eupteris” (nom. inval. = P. sect. Pteris), P. sect. Heterophlebium (Fee) Hook. and P. sect. Litobrochia (C. Presl) Hook. were accepted, and later three subgenera “P. subg. Eupteris” (= P. subg. Pteris), P. subg. Campteria (C. Presl) C. Chr., and P. subg. Litobrochia (C. Presl) C. Chr., were proposed. In spite of the obvious artificiality of Christensen’s (1906) infrageneric classification (Walker, 1962), many more recent taxonomic studies have adopted it to a large extent (e.g. Wu, 1990; Yang, 2011; Liao et al., 2013). The earliest competitor to Christensen’s system was that of Shieh (1966), who emphasized the importance of patterns of leaf architecture and proposed a reclassification into two subgenera, P. subg. Pteris (leaves pinnate or bipinnate) and P. subg. Tripedipteris W. C. Shieh (leaves tripartite), with the two subgenera each divided into two sections: P. subg. Pteris into P. sect. Pteris and P. sect. Campteria (C. Presl) Hook., and P. subg. Tripedipteris into P. sect. Hypsopodium W. C. Shieh and P. sect. Tripedipteris W. C. Shieh. Combining the patterns of frond architecture and venation type, Tryon and Tryon (1982) divided the Neotropical species of Pteris into six unranked groups. Finally, in classifying species of Pteris of China, Ching and Wu (1983) recognized three sections, P. sect. Pteris, P. sect. Campteria and P. sect. Quadriauricula Ching, with the last two each further divided into two series. Ching and Wu’s classification was adopted in a recent taxonomic treatment in Flora of China (Liao et al., 2013). Although the generic relationships within the Pteridaceae subfamily Pteridoideae have frequently been explored based on DNA sequences of one (Nakazato and Gastony, 2003; Li et al., 2004; S anchez-Baracaldo, 2004b; Prado et al., 2007; Schuettpelz et al., 2007; Bouma et al., 2010; Schneider et al., 2013; Cochran et al., 2014), or three or four (Schuettpelz et al., 2007; Cochran et al., 2014) plastid genes, there have been very few studies focusing on the relationships within Pteris. Li et al. (2004) used trnL-F intergenic spacer sequences (< 400 base pairs) from 16 Chinese species to reconstruct the first phylogeny of Pteris, and concluded that Pteris was strongly supported as monophyletic and that P. vittata L. was resolved as the earliest diverging lineage. However, Platyzoma R. Br. was not sampled and only one distantly related outgroup, Adiantum capillus-veneris L., was included in their analysis. Using rbcL gene sequences of 10 species of Pteris and related genera in Pteridaceae, Prado et al. (2007) found that Pteris was paraphyletic in relation to Platyzoma, a monospecific Australian endemic. Based on atpA, atpB and rbcL gene data from nine species of Pteris and a broad sampling of related genera, Schuettpelz et al. (2007) discovered that Pteris was also paraphyletic with respect to Neurocallis Fee (a Neotropical monospecific genus), Ochropteris J. Sm. (a Malagasy and Mascarene bispecific genus), and Platyzoma. Most interestingly, Schuettpelz et al. (2007) found that P. vittata, a species morphologically similar to the type of the genus (P. longifolia L., not sampled in their study), was not resolved as closely allied to the remainder of the genus. They suggested that the definition of Pteris would need to be expanded to include their entire “pteridoid clade” (Rothfels, 2008) or reduced to the small clade of P. longifolia, P. vittata and their close allies. More recent studies of the Pteridaceae (e.g. Bouma et al., 2010; Chao et al., 2012a; Jaruwattanaphan et al., 2013; Schneider et al., 2013) have provided only limited information concerning the phylogeny of Pteris. To date, there have not been any large-scale multilocus molecular phylogenetic studies of Pteris. Pteris is normally placed in the subfamily Pteridoideae. The circumscription of the latter, however, has been controversial: Tryon et al. (1990) placed five genera in the Pteridoideae and 13 genera in the Taenitidoideae; Sanchez-Baracaldo (2004b) rejected the monophyly of the Taenitidoideae sensu Tryon et al. (1990) using rps4-trnS data; Smith et al. (2006) combined the two subfamilies; Schuettpelz et al. (2007) suggested that the Taenitidoideae lineage was nested within the Pteridoideae. The sampling of taxa and/or characters so far has been limited. The objectives of this study were: (i) to resolve the relationships within the Pteridoideae; (ii) to test the monophyly of Pteris with the largest taxon and character sampling so far utilized, including the type of the genus, P. longifolia; (iii) to better resolve the relationships of the enigmatic genus Platyzoma; (iv) to identify major evolutionary lineages within Pteris and L. Zhang et al. / Cladistics (2014) 1–18 the position of its type species; (v) to evaluate previous morphological hypotheses about the relationships within Pteridaceae subfamily Pteridoideae; and (vi) to understand morphological features for the resolved lineages. 3 South China Botanical Garden, Chinese Academy of Sciences (IBSC), Kunming Institute of Botany, Chinese Academy of Sciences (KUN), Missouri Botanical Garden (MO), Yunnan University (PYU). DNA extraction, amplification and sequencing Materials and methods Taxon sampling The taxa were sampled to include representatives of each of the four sections recognized by Hooker and Baker (1874) and Christensen (1906), the four sections and seven subsections proposed by Shieh (1966), the six unranked groups defined by Tryon and Tryon (1982), and the three sections and four series circumscribed by Ching and Wu (1983). The generic type, P. longifolia, is included for the first time. In total, Pteris sensu lato was represented by 105 accessions of 84 species from four continents, including one accession of Afropteris barklyae (Baker) Alston, two of Neurocallis praestantissima Bory ex Fee and one of Ochropteris pallens (Sw.) J. Sm. To test the monophyly of Pteris and its relationships within the Pteridoideae, 38 accessions of 15 additional genera in Pteridoideae and Taenitidoideae sensu Tryon et al. (1990), including a newly described genus, Tryonia Schuettp., J. Prado & A. T. Cochran, segregated from Eriosorus Fee and Jamesonia Hook. & Grev. (Cochran et al., 2014), were included based largely on the results of Schuettpelz et al. (2007). Eriosorus and Platyzoma were treated as two independent genera. In total, our ingroup comprised 142 accessions representing 116 species in 16 genera of the Pteridoideae. One species each of Adiantum L., Ceratopteris Brongn. and Acrostichum L. were used as outgroups, given that the Ceratopteridoideae (comprising Acrostichum and Ceratopteris) was resolved as sister to the Pteridoideae and that Adiantum is in a clade that is a further sister to the clade containing the Ceratopteridoideae and the Pteridoideae (Prado et al., 2007; Schuettpelz et al., 2007). Voucher information and GenBank accession numbers for each sampled taxon are provided in Appendix 1. Morphology Morphological data were obtained from field observations, herbarium investigations and literature study (see ‘Discussion’ below for references), field observations were mainly conducted by the first author in China, Myanmar and Vietnam, and herbarium investigations were carried out at herbaria Chengdu Institute of Biology, Chinese Academy of Sciences (CDBI), Total genomic DNA was extracted from silica-dried material or sometimes from herbarium specimens using a Tiangen Biotech plant genomic DNA extraction kit (Beijing, China) or DNeasy Plant Mini Kits (Qiagen, D€ usseldorf, Germany) following the manufacturers’ protocols. Six plastid regions (the atpA gene, the atpB gene, the rbcL gene, the rps4-trnS intergenic spacer, the trnL intron and the trnL-F intergenic spacer) were selected based on their use in earlier studies of the Pteridaceae (Nakazato and Gastony, 2003; Prado et al., 2007; Schuettpelz et al., 2007; Rothfels et al., 2008; Bouma et al., 2010; Lu et al., 2012; Sigel et al., 2011). The atpA gene was amplified with primers ESATPF412F and ESTRNR46F (Schuettpelz et al., 2006) and the atpB gene with primers ESATB672F and ESATPE384R (Pryer et al., 2004). Most rbcL sequences were amplified with primers F1 (Fay et al., 1997) and 1379R, originally designed by Zurawski et al. (1984) and modified by Wolf et al. (1999). For some herbarium specimens with degraded DNA, newly designed internal primers of rbcL gene 595F (50 -AAT TCYCARCCRTTCATGCGT-30 ), 650R (50 -AGAGCTTCYGCYACRAATA-30 ) and 819R (50 -AGCTA AGCTGGTRTTKGCRGT -30 ) were used when amplification of the larger region was unsuccessful. The rps4-trnS intergenic spacer was amplified with primers TRNS (Souza-Chies et al., 1997) and an anonymous primer derived from Li and Lu (2006). The trnL intron and trnL-F intergenic spacer were amplified together using the primers FERN1 (Trewick et al., 2002) and F (Taberlet et al., 1991). The PCR conditions followed Zhang et al. (2001). Amplified fragments were purified with TIANquick Mini Purification Kits (Tiangen Biotech) and purified polymerase chain reaction (PCR) products were sequenced by Invitrogen (Shanghai, China). Sequence alignment and phylogenetic analysis Sequencher 4.1 (Gene Codes Corp., Ann Arbor, MI, USA) was used to assemble and edit complementary strands. Sequences obtained for each locus were aligned individually using Clustal X 1.81 (Thompson et al., 1997) followed by manual adjustments using BioEdit (Hall, 1999). Partial regions of the rps4-trnS spacer and trnL-F spacer of several genera (such as Pityrogramma Link) were removed prior to analysis, because they were highly divergent and difficult to align with Pteris. G, gamma-distribution-shape parameter (Yang, 1994); GTR, general-time-reversible model (Tavare, 1986); I, proportion of invariable sites; Ti/Tv, transition/transversion ratio. 0.2920 0.9650 0.8570 0.6110 0.9170 1.7710 1.0850 0.3220 0 0.5970 0.5500 0 0 0 0 0 – – – – – – – – 1.0000 1.0000 1.0000 1.0000 1.0000 1.0000 1.0000 1.0000 6.8240 5.6368 3.8994 2.4720 1.9001 1.8990 1.8974 3.5402 0.6820 0.7985 0.4392 0.6261 0.4233 0.6506 0.5172 0.5464 0.4339 0.6786 0.8251 0.3072 0.5364 0.4123 0.4835 0.5937 4.0668 6.2772 4.3946 2.5069 2.1279 2.0845 2.0827 3.4344 1.0765 1.6928 0.7584 0.9610 0.9324 0.8258 0.8775 1.0281 0.3045 0.2934 0.2764 0.3001 0.3150 0.3150 0.3129 0.2951 0.1964 0.2201 0.2211 0.1805 0.1762 0.1622 0.1712 0.2012 0.1775 0.1959 0.2312 0.1575 0.1558 0.1721 0.1636 0.1886 + + + + + + + + G I+G I+G I+G G G G G GTR GTR GTR GTR GTR GTR GTR GTR atpA gene atpB gene rbcL gene rps4-trnS spacer trnL intron trnL-F spacer trnL intron and trnL-F spacer Simultaneous 0.3217 0.2907 0.2714 0.3618 0.3531 0.3507 0.3523 0.3151 I Ti/tv G–T C–T C–G A–T A–G A–C T Substitution model (rate matrix) G C A Selected model This study generated 573 new sequences (Appendix 1). The dataset characteristics and tree statistics Region Results Base frequencies Equally weighted maximum-parsimony (MP) analyses were conducted for each locus using 1000 tree-bisection-reconnection (TBR) searches in PAUP* version 4.0b10 (Swofford, 2002) with MAXTREES set to increase without limit. Insertions and deletions were coded as missing data. Parsimony jackknife (JK) analyses (Farris et al., 1996) were conducted using PAUP* with the removal probability set to approximately 37%, and “jac” resampling emulated. Two thousand replicates were performed with ten TBR searches per replicate and a maximum of 100 trees held per TBR search. jModelTest 0.1.1 (Guindon and Gascuel, 2003; Posada, 2008) was used to select the best-fitting likelihood model for maximum likelihood (ML; Felsenstein, 1973) analyses. The Akaike information criterion (Akaike, 1974) was used to select among models instead of the hierarchical likelihood ratio test, following Pol (2004) and Posada and Buckley (2004). The best-fitting models and parameter values are provided in Table 1. For each locus and the simultaneous analysis (Kluge, 1989; Nixon and Carpenter, 1996) of all nucleotide characters, ML tree searches and ML bootstrapping were conducted using the web server RAxML-HPC2 on TG version 7.2.8 (Stamatakis et al., 2008; Miller et al., 2010) with 5000 rapid bootstrap analyses followed by a search for the best-scoring tree in a single run (Stamatakis et al., 2008). Well-supported (≥ 70% JK or BS support; Zhang and Simmons, 2006; Zhang et al., 2012) clades that conflicted with one another in the parsimony JK and likelihood BS trees were then tested for long-branch attraction (Felsenstein, 1978) by alternatively removing the terminals in question. If the terminal(s) remaining in the parsimony analysis moved to a different part of the tree (with ≥ 70% JK support) when the potentially attracting terminal(s) were removed, the result was consistent with the explanation of long-branch attraction (Siddall and Whiting, 1999; Zhang and Simmons, 2006). Bayesian inference (BI) was conducted using MrBayes 3.1.2 (Huelsenbeck and Ronquist, 2001; Ronquist and Huelsenbeck, 2003) on Cipres (Miller et al., 2010). Four Markov chain Monte Carlo chains were run, each beginning with a random tree and sampling one tree every 1000 generations of 10 000 000 generations. Convergence among generations was checked using Tracer (Rambaut and Drummond, 2007) and the first 25% was discarded as burn-in to ensure that stationarity in log-likelihood had been reached. The remaining trees were used to calculate a 50% majority-rule consensus topology. G L. Zhang et al. / Cladistics (2014) 1–18 Table 1 Best-fitting models and parameter values for separate (atpA, atpB, rbcL, rps4-trnS, trnL, trnL-F, and trnL & trnL-F) and simultaneous plastid datasets in this study 4 L. Zhang et al. / Cladistics (2014) 1–18 for the analyses are presented in Table 2. Comparisons of tree topologies from the MP JK analyses of the individual markers identified no well-supported conflicts (JK ≥ 70%; Mason-Gamer and Kellogg, 1996; Zhang and Simmons, 2006; Zhang et al., 2012). Thus, the six plastid datasets were concatenated. The topology of the ML tree based on the combined dataset (Fig. 1a, b) was mostly identical to those based on each individual marker, but with generally increased support values. The topologies and support values from ML and MP analyses were similar except for the position of Platyzoma. The MP analysis resolved Platyzoma as sister to the rest of Pteridoideae, with maximum support values and a long branch. In contrast, the BI and ML analyses resolved Platyzoma as sister to the rest of Pteris superclade A (Fig. 1b), but support values were low. This well-supported conflict could point to long-branch attraction (Bergsten, 2005; Zhang and Simmons, 2006). We then conducted tests of long-branch attraction (Siddall and Whiting, 1999) by repeating BI, ML BS and MP JK analyses with the following six removals, because these groups had the longest branches in the ML analysis (Schuettpelz et al., 2007; Fig. 1a): Acrostichum, Adiantum, Ceratopteris, Acrostichum + Ceratopteris, Acrostichum + Adiantum and Acrostichum + Adiantum + Ceratopteris. Our tests showed that when these three genera were all removed, all BI, ML BS and MP JK analyses resolved Platyzoma as sister to clades II and III with relatively strong BI PP (100%), ML BS (96%) and MP JK support (78%), consistent with the result of BI and ML analyses of the full taxon sample. The monophyly of the Pteridoideae was maximally supported in all BI, ML and MP analyses, which helped confirm the Pteridoideae as a natural group (Fig. 1a). Pteris plus Platyzoma (when the long-branch attraction artefact was avoided) was resolved as monophyletic with strong support (ML BS 100%, PP 100%, MP JK 97%) and as sister to the rest of the ingroup. The phylogenetic relationships among the remaining genera were well resolved (Fig. 1a, b). Species of Eriosorus were nested within Jamesonia (Fig. 1a). Cerosora microphylla (Hook.) R.M.Tryon [Anogramma microphylla (Hook.) Diels] was more closely related to Pityrogramma than to A. guatemalensis (Domin) C. Chr. and A. leptophylla (L.) Link. Based on our reconstructed phylogeny (Fig. 1a, b) and in consideration of morphological characters and distribution information, 15 clades representing 15 major evolutionary lineages of Pteris were identified (Fig. 1b). All 15 clades were well supported (14 were supported by ML BS ≥ 98, PP = 100% and MP JK ≥ 99%, and one by ML BS = 79%, PP = 100% and MP JK = 84%). The relationships among most of the 15 clades were also well supported. Three additional supported monophyletic superclades within the 5 15 clades were named for descriptive convenience. Superclade A (BS = 96%, PP = 100%, JK = 78%) contains clades I–III; Superclade B (BS = 100%, PP = 100%, JK = 100%) comprises clades V–IX; and Superclade C (well supported only by BS = 72%; PP = 77%,) contains clades X–XV. Discussion Circumscription of Pteridoideae Pteridaceae subfamily Pteridoideae sensu Tryon et al. (1990) contains Acrostichum, Anopteris (Prantl) Diels, Neurocallis, Ochropteris and Pteris. Acrostichum should be excluded from Pteridoideae based on the findings by Prado et al. (2007) and Schuettpelz et al. (2007). The monospecific genus Anopteris has not been included in any molecular studies so far. It resembles Pteris morphologically in having sporangia grouped into submarginal sori (Tryon et al., 1990). Whereas it might well be a member of Pteris, Neurocallis and Ochropteris undoubtedly are (see ‘Discussion’ below; Fig. 1b: clades VII, XI). The Pteridoideae sensu Tryon et al. (1990) excluding Acrostichum is basically Pteris in our definition below. The subfamily Taenitidoideae sensu Tryon et al. (1990) contains 13 genera: Actiniopteris, Afropteris Alston, Anogramma Link, Austrogramme E. Fourn., Cerosora Baker, Eriosorus, Jamesonia, Nephopteris Lellinger, Onychium Kaulf., Pityrogramma, Pterozonium Fee, Syngramma J. Sm. and Taenitis Willd. ex Schkuhr. Our study shows that the Taenitidoideae sensu Tryon et al. (1990) is paraphyletic in relation to Pteris sensu lato because Afropteris is resolved as part of Pteris (Fig. 1b). One genus included in the Taenitidoideae sensu Tryon et al. (1990), Nephopteris, was not sampled in our study. The Taenitidoideae, if recognized, should exclude Afropteris but include Cosentinia Tod. and the newly described Tryonia (Fig. 1a). Cosentinia was synonymized with Cheilanthes Sw., which was included in the Cheilanthoideae by Tryon et al. (1990). Our results (Fig. 1a, b) indicate that a monophyletic Pteridoideae sensu stricto comprising only Pteris could be recognized, with the Taenitidoideae containing the rest of our ingroup. Here, following the broader circumscription sensu Smith et al. (2006) we adopt the Pteridoideae sensu lato to include both of these clades. The Pteridoideae in our definition contains 15 genera: Actiniopteris Link, Anogramma, Austrogramme, Cerosora, Cosentinia, Eriosorus, Jamesonia, Nephopteris, Onychium, Pityrogramma, Pteris, Pterozonium, Syngramma, Taenitis and Tryonia. In comparison with its sister group the Ceratopteridoideae (Schuettpelz et al., 2007), which has sporangia distantly on veins (Tryon et al., 1990), members of the Pteridoideae have spo- 6 L. Zhang et al. / Cladistics (2014) 1–18 rangia approximate and in sori or soral lines on veins or on a marginal commissure (Tryon et al., 1990). Phylogeny of Pteridoideae The monophyly of the Pteridoideae as defined above is confirmed by our study with strong support (Fig. 1a, b). Pteris together with Afropteris, Neurocallis, Ochropteris and Platyzoma (see ‘Discussion’ below) was resolved as sister to the remaining genera of the Pteridoideae. Although the overall relationships determined are not in conflict with those inferred by Schuettpelz et al. (2007) or Cochran et al. (2014), our greater taxon and character sampling resulted in better support. The sister relationship between Actiniopteris and Onychium (Prado et al., 2007; Schuettpelz et al., 2007; Schneider et al., 2013) is also recognized in our study (BS = 100%, PP = 100%, JK = 100%). The two genera share the morphological features of sporangia in a soral line in a marginal commissure covered by a well-developed marginal indusium. The Actiniopteris + Onychium clade is strongly supported as sister to the remaining non-Pteris genera in Pteridoideae (Fig. 1a, b), a relationship consistent with earlier (a) studies (Schuettpelz et al., 2007; Schneider et al., 2013); our study is the first to provide strong support for this relationship. Marginal commissural veins also appear in Pteris. Based on our phylogeny, it is equally parsimonious to hypothesize that this character state either evolved once in the common ancestor of the Pteridoideae or independently evolved twice in Pteris and in the Actiniopteris + Onychium clade. Our data resolved the recently described genus Tryonia as sister to a clade containing Austrogramme, Syngramma and Taenitis, and these three together are sister to Pterozonium (Fig. 1a, b), a resolution consistent with findings by Cochran et al. (2014). Nakazato and Gastony (2003) provided the first molecular evidence that Anogramma, as traditionally circumscribed, is highly paraphyletic, with everything except A. leptophylla (and A. guatemalensis) moved to other genera, including Eriosorus, Pityrogramma, etc. Our results confirm the polyphyly of Anogramma. Schneider et al. (2013) transferred a portion of Anogramma to Cerosora. Previous studies were uncertain about the distinctiveness of A. guatemalensis from A. leptophylla (Tryon, 1962; Gastony and Baroutsis, 1975; Smith, 1981; Mickel and Smith, 2004), however, there was an amplified fragment Pteris (see Fig. 1b) Pteridoideae Onychium contiguum Onychium japonicum Actiniopteris dimorpha Actiniopteris semiflabella Acrostichum danaeifolium Acrostichum danaeifolium Adiantum capillusveneris Cosentinia vellea Anogramma leptophylla Anogramma guatemalensis Cerosora (Anogramma) microphylla Pityrogramma ebenea Pityrogramma jamesonii Pityrogramma sp. Pityrogramma austroamericana Pityrogramma presliana Pityrogramma calomelanos Pityrogramma calomelanos Pityrogramma ochracea Pityrogramma trifoliata Eriosorus flexuosus Eriosorus flexuosus Eriosorus cheilanthoides Eriosorus elongatus Eriosorus hirtus Jamesonia scammaniae Jamesonia goudotii Jamesonia verticalis Jamesonia verticalis Pterozonium brevifrons Pterozonium brevifrons Pterozonium reniforme Austrogramme decipiens Austrogramme marginata Syngramma quinata Taenitis blechnoide Taenitis interrupta Tryonia myriophylla Tryonia myriophylla Ceratopteris richardii 0.04 substitutions/site Fig. 1. (a) Maximum likelihood phylogeny of the Pteridoideae based on six plastid regions (atpA, atpB, rbcL, rps4-trnS, trnL and trnL-F) (ln = 45 767.2102). Thickest lines indicate strong support [maximum parsimony jackknife support (MP JK) ≥ 75%, maximum likelihood bootstrap support (ML BS) ≥ 75% and Bayesian inference posterior probability (BI PP) ≥ 95%)], medium lines indicate moderate support (either ML BS ≥ 75% or BI PP ≥ 95%), and thin lines indicate weak support (ML BS ≤ 75% and BI PP ≤ 95%). Dashed branches indicate those that have been truncated. The 15 major clades of Pteris resolved in this study are indicated. In (b) the major diagnostic morphological features are shown in green and geographical provenances of samples of Pteris are indicated in blue. (Colour online) L. Zhang et al. / Cladistics (2014) 1–18 length polymorphism (AFLP) study of populations in the complex showing a high genetic identity of A. guatemalensis with A. leptophylla, especially the 7 sample from Mexico (Nakazato and Gastony, 2003). Our data suggest that the two taxa are distinct (23 nucleotide differences in rbcL and rps4-trnS) and that (b) Superclade C Superclade B Superclade A P. nanlingensis Guizhou, China P. japonica Taiwan, China P. esquirolii Guizhou, China P. cretica Yunnan, China P. umbrosa Atherton, Australia P. umbrosa cult. in Atherton, Australia P. deltodon Sichuan, China P. xiaoyingiae Guangxi, China P. actiniopteroides Sichuan, China P. gallinopes Guizhou, China P. henryi Guizhou, China P. dactylina Sichuan, China P. multifida Selangor, Malaysia P. multifida Guayas, Ecuador P. multifida Jiangxi, China P. morii Hainan, China P. morii Haina n, China P. pseudopellucida Louangphrabang, Laos P. sp. Sulawesi Tenggara, Indonesia P. mutilata Puerto Rico P. pungens Heredia, Costa Rica P. usambarensis Taita-Taveta, Kenya P. commutata Buliisa, Uganda P. burtonii Buliisa, Uganda P. navarrensis San José, Costa Rica P. livida Napo, Ecuador P. decurrens São Paulo, Brazil P. deflexa Rio de Janeiro, Brazil P. muricata Pichincha, Ecuador Rio Grande do Sul., Brazil P. deflexa P. altissima Alajuela, Costa Rica P. chiapensis Chiapas, Mexico cult. in UC Berkeley Bot. Gard., USA P. altissima P. speciosa Alajuela, Costa Rica P. haenkeana Pasco, Peru P. podophylla Pichincha, Ecuador P. orizabae Chiapas, Mexico P. dentata La Réunion, France P. finotii Hainan, China P. wallichiana var. wallichiana Guangdong, China P. wallichiana var. yunnanensis Yunnan, China P. arborea Guadeloupe P. tripartita cult. in Atherton, Australia P. tripartita cult. in Bot. Gart. Berlin-Dahlem, Germany P. buchananii Chogoria, Kenya P. saxatilis New Zealand P. comans New Zealand P. macilenta New Zealand P. microptera Lord Howe Island, Australia P. (Ochropteris) pallens La Réunion, France P. (Afropteris) barklyae Seychelles Paraná, Brazil P. lechleri P. lechleri São Paulo, Brazil P. propinqua Zamora-Chinchipe, Brazil P. splendens São Paulo, Brazil P. brasiliensis São Paulo, Brazil São Paulo, Brazil P. denticulata P. denticulata Rio de Janeiro, Brazil P. leptophylla São Paulo, Brazil P. linearis Hainan, China P. linearis La Réunion, France P. setulosocostulata Sichuan, China P. catoptera Samburu, Kenya Masindi, Uganda P. preussii P. quadriaurita cult. in Alter Bot. Gart., Germany P. friesii Kagera, Tanzania P. griffithii Kachin, Myanmar P. biaurita Nan, Thailand Hainan, China P. biaurita P. splendida Guangxi, China P. pacifica cult. in Atherton, Australia P. viridissima Guizhou, China P. puberula Yunnan, China Louangphrabang, Laos P. heteromorpha Kachin, Myanmar P. pellucida P. decrescens Guangxi, China P. decrescens Guizhou, China P. cadieri Guangdong, China P. grevilleana Hainan, China P. quadristipitis Guizhou, China Guadeloupe, France P. (Neurocallis) praestantissima P. (Neurocallis) praestantissima Heredia, Costa Rica P. fraseri Napo, Ecuador P. terminalis Sichuan, China P. insignis Guangdong, China P. ensiformis cult. in Australia P. ensiformis Yunnan, China P. bella Hainan, China P. bella Guangdong, China P. amoena Tibet, China P. mcclurei Guangdong, China Hainan, China P. longipes Yunnan, China P. longipes P. semipinnata Sichuan, China Guangdong, China P. dimidiata P. dimidiata Pahang, Malaysia P. chilensis Limache, Chile P. tremula cult. in Australia P. tremula cult. in Australia P. vittata Florida, USA cult. in Australia P. vittata Sichuan, China P. vittata P. longifolia Guerrero, Mexico P. bahamensis Florida, USA P. grandifolia Huehuetenango, Guatemala Platyzoma microphyllum rest of Pteridoideae (see Fig. 1a) 0.04 substitutions/site Fig. 1b. Continued XV Veins free, frond often dimorphic, lamina pedate, pinnatifid or pinnate, pinnae never pectinate Terminal or lateral pinna conspicuously XIV decurrent XIII Native to South America, veins areolate (except P. deflexa and P. muricata) XII Lamina herbaceous, pinnae pectinate, length-width ratio of pinnules of middle part of pinnae ca. 5:1 XI Large habit, veins areolate (except P. barklyae and P. pallens ) X Native to South America, veins areolate IX Veins free (except P. biaurita), pinnae pectinate, basal pairs of pinnae with 1–3 (or 4) pinnules near base at basiscopic side VIII Veins free, lamina 1-pinnate to 2-pinnatifid VII Length-width ratio of lateral pinnae or pinnules ca. 5:1 or larger VI Native to Asia, pinnae pectinate, veins free (except P. mcclurei) V Veins free, pinnae pectinate, acroscopic pinnae entire, subentire or lobed Veins free, lamina 3-pinnate to 4-pinnatifid IV III II I Veins free, lamina 1-pinnate, lanceolate Length-width ratio of costal areolae ca. 5:1 or larger Heterosporous condition 8 L. Zhang et al. / Cladistics (2014) 1–18 A. guatemalensis might be recognized taxonomically at some rank. Cerosora, Platyzoma and all members of the lower clade of Fig. 1a (Austrogramme, Eriosorus, Jamesonia, Pterozonium, Syngramma, Taenitis and Tryonia) bear trichomes or bristles instead of scales on rhizome or stem (Tryon et al., 1990). Based on our phylogeny (Fig. 1a, b), trichomes or bristles appear to have evolved from scales three times independently in these three clades. Additional important relationships in the Pteridoideae will be discussed below. Resolution of Pterozonium Copeland (1947) suggested that the morphologically variable South American genus Pterozonium might be related to Eriosorus and Jamesonia. Our study found instead that Pterozonium is sister to a clade containing Austrogramme, Syngramma, Taenitis and Tryonia. The sister genera Austrogramme and Syngramma are together sister to Taenitis, which is consistent with the findings of S anchez-Baracaldo (2004b), who did not sample species of Tryonia. In comparison with Taenitis (which has veins anastomosing from costa to margins or rarely only costal areolae present), both Austrogramme and Syngramma have veins joined only at the margin or in one or two series of marginal areolae. Biogeographically, these five genera are distributed pantropically from India (to Fiji; Taenitis), Malesia to the Pacific islands (Austrogramme and Syngramma) and to South America (Pterozonium and Tryonia). Resolution of Eriosorus and Jamesonia Austrogramme, Pterozonium, Syngramma, Taenitis and Tryonia together are sister to a clade comprising Eriosorus (five species sampled) and Jamesonia (four species sampled) (Fig. 1a, b). Notably, Jamesonia as currently circumscribed is paraphyletic in relation to a monophyletic Eriosorus, a resolution different from the rps4 phylogeny of S anchez-Baracaldo (2004a) and the rbcL phylogeny of Schuettpelz et al. (2007), where both genera were found to be paraphyletic in relation to each other. However, our resolution is consistent with that found by Cochran et al. (2014), who placed species of Eriosorus in Jamesonia. Based on our result, simply transferring J. scammaniae A. F. Tryon to Eriosorus would make both genera monophyletic (Fig. 1a) in our current sampling. However, our taxon sampling of the two genera is much smaller than that of S anchez-Baracaldo (2004a) but we have much larger character sampling. In order to resolve the relationships between Eriosorus and Jamesonia it is desirable to have larger sampling of both taxa and characters. Resolution of Neurocallis Neurocallis comprises only N. praestantissima, an uncommonly collected species with a discontinuous distribution in the Neotropics (Christensen, 1934; Copeland, 1947; Wagner, 1980; Tryon et al., 1990). Leaves of N. praestantissima are dimorphic, singly pinnate and have anastomosing veins. Based on the nearly acrostichoid fertile fronds, some authors treated the genus as a synonym of Acrostichum (e.g. Christensen, 1906). Wagner (1980) found that the chromosome number (n = 58) of Neurocallis is consistent with Pteris and the leaves have some similarities to those of P. grandifolia L., and he suggested a closer relationship between Neurocallis and Pteris. Schuettpelz et al. (2007) showed that N. praestantissima should be included in Pteris and was sister to a clade containing P. argyraea T. Moore, P. fauriei Hieron. and P. quadriaurita Retz. Our study supports the inclusion of Neurocallis in Pteris but found that it is more closely related with P. fraseri Mett. ex Kuhn than with P. grandifolia or the P. quadriaurita complex (Fig. 1b: clade VII). Pteris fraseri is distributed in tropical montane forests of Ecuador and Peru. The remarkable morphological characters of P. fraseri include the tall habit, large sterile fronds of more than 2 m long and the ultimate pinnae ternate—long, entire and remotely spaced. However, the species has dimorphic fronds, sterile fronds much wider than fertile fronds, anastomosing veins, and entire pinna margins, which are comparable to N. praestantissima. Resolution of Afropteris and Ochropteris According to Alston (1956), Afropteris consists of two species: A. repens (C. Chr.) Alston in tropical West Africa and A. barklyae, which is endemic to the Seychelles. Tryon et al. (1990) placed Afropteris in the Pteridaceae subfamily Taenitidoideae. Ochropteris is a small tropical genus occurring in Madagascar and the nearby Seychelles and Mascarenes; O. bosseri Tardieu, O. pallens and O. peltigera Fee are typically recognized, although some authors have treated O. bosseri and O. peltigera as synonyms of O. pallens (e.g. Tardieu-Blot, 1958; Autrey et al., 2008). Before the genus was described, O. pallens was placed in Adiantum, Cheilanthes Sw. or Cryptogramma R. Br. When Smith (1841) published Ochropteris, he recognized that the morphology of the sori was similar to that of Pteris, but that the habit was inconsistent with any species of Pteris. Tryon and Tryon (1982) noted that Afropteris and Ochropteris were doubtfully distinct from Pteris and Tryon et al. (1990) placed Ochropteris in the Pteridaceae subfamily Pteridoideae. Using single plastid sequence data rps4-trnS Sanchez-Baracaldo (2004b) found that A. barklyae was nested within Pteris—simi- L. Zhang et al. / Cladistics (2014) 1–18 lar results to those found by Schuettpelz et al. (2007) using rbcL data. Our study confirms their findings and further reveals the sister relationship between Ochropteris and Afopteris (Fig. 1b: clade XI). Although the habits of the two taxa are quite different from other species of Pteris, they are morphologically similar to each other in having the long-creeping rhizome, lamina herbaceous and three-pinnate to four-pinnatifid, and fine ultimate pinnules. Resolution of Platyzoma The genus Platyzoma contains only the striking species P. microphyllum, which is endemic to northern Australia (Brown, 1810). Due to its anomalous morphology (narrowly linear single-pinnate fronds, presence of abundant farina, and incipient heterospory), the systematic position of the species has long been controversial. The initial studies tended to treat it as a genus of Gleicheniaceae allied to Gleichenia Link (Brown, 1810; Presl, 1836; Moore, 1857; Hooker and Baker, 1874), or as a species of Gleichenia (Christ, 1897; Christensen, 1906). Thompson (1917) provided detailed data on anatomy of the species but still treated it in Gleicheniaceae. However, he suggested that its close affinity with Gleichenia was dubious. Nakai (1950) proposed a monospecific family Platyzomataceae, which was adopted by Bostock et al. (1998). Tryon (1961, 1964) placed Platyzoma in the Polypodiaceae subfamily Platyzomatoideae and later (Tryon and Tryon, 1982) in the Pteridaceae tribe Platyzomateae or the Pteridaceae subfamily Platyzomatoideae (Tryon et al., 1990). Hasebe et al. (1994), who sampled 12 species in 11 genera of Pteridaceae, first resolved Platyzoma as a member of Pteridaceae based on a singlelocus dataset of rbcL. In their study, Platyzoma and Taenitis were resolved as sister to each other. Based on the same rbcL sequence (Prado et al., 2007; Bouma 9 et al., 2010) or combined with data of two additional plastid genes, atpA and atpB (Schuettpelz et al., 2007), the inclusion of Platyzoma in Pteridaceae was confirmed, but its precise phylogenetic relationships remained unresolved. In our analysis, the inclusion of Platyzoma in Pteridoideae is strongly supported. With the three long-branched attracting genera removed, our BI, ML and MP analyses of six-gene data resolved Platyzoma as being nested within Pteris and as sister to clade II (P. grandifolia) + clade III [P. longifolia/ P. bahamensis (J. Agardh) Fee and P. vittata; Fig. 1b]. This resolution received relatively high BS (96%), PP (100%) and JK (78%) support in ML, BI and MP analyses, respectively. Notably, the effect of longbranch attraction was neglected by all previous studies when Platyzoma was involved (Hasebe et al., 1994; Prado et al., 2007; Schuettpelz et al., 2007; Schneider et al., 2013). Interestingly, all species of superclade A (clades I–III; Fig. 1b) have single-pinnate lanceolate/ linear lamina, which might be interpreted as a morphological synapomorphy of superclade A. Platyzoma microphyllum is the only non-aquatic fern with a heterosporous condition. In about 11 000 species of ferns, heterospory occurs in only six genera: Azolla Lam., Marsilea L., Pilularia L., Regnellidium Lindm., Salvinia Seg. (aquatic ferns) and Platyzoma. Similar to habitats of other heterosporous ferns, P. microphyllum primarily grows in deep granitic sand that overlies heavy clay and is often flooded in the rainy season (Tryon et al., 1990). Adaption to wet conditions might have driven the evolution of heterospory in all these ferns. Monophyly of Pteris Our analyses showed that Pteris in its current circumscription is paraphyletic in relation to Afropteris, Neurocallis, Ochropteris and Platyzoma (Fig. 1b). This resolution is consistent with the results of earlier stud- Table 2 Data matrices and tree statistics for each of the analyses Matrix rbcL gene atpB gene atpA gene rps4-trnS spacer trnL intron trnL-F spacer trnL intron and trnL-F spacer Simultaneous Number of accessions Number of characters 139 127 129 127 113 113 114 1286 1189 1819 1018 755 466 1221 146 6534 Number of PI characters (%)* MPT length Number of MPTs Number of MP JK/ML BS clades Average MP JK/ML BS support (%) CI RI (26.2) (25.0) (29.0) (39.5) (42.3) (50.6) (45.5) 1334 1104 1816 1277 1006 831 1846 1 1 1 1 2 1 2 800 400 100 600 100 500 200 93/105 76/86 92/96 100/100 75/85 78/80 91/98 85/86 85/87 89/91 87/88 85/87 81/85 89/89 0.4303 0.4457 0.5061 0.5732 0.5895 0.5620 0.5742 0.8177 0.8234 0.8447 0.8612 0.8693 0.8436 0.8568 2199 (33.7) 7442 1 676 700 129/136 93/94 0.5075 0.8394 338 297 528 402 319 236 555 791 899 971 864 015 989 016 PI, parsimony-informative; MPT, most parsimonious trees; MP, maximum parsimony; ML, maximum likelihood; JK, jackknife; BS, bootstrap; CI, consistency index; RI, retention index. * Inclusive of outgroups. 10 L. Zhang et al. / Cladistics (2014) 1–18 ies using limited character and taxon sampling (S anchez-Baracaldo, 2004a; Prado et al., 2007; Schuettpelz et al., 2007; Schneider et al., 2013). Our study provides the first strong molecular evidence that the Australian endemic Platyzoma, along with Afropteris, Neurocallis and Ochropteris, is embedded in Pteris sensu lato. At this stage we advocate a broad circumscription of Pteris that includes these smaller genera (Afropteris, Neurocallis, Ochropteris and Platyzoma each contain only one to three species; names for all the taxa are already available in Pteris (Zhang et al., 2014)) in order to maintain maximum nomenclatural stability (Pteris comprises about 200–250 species, most of which would require new names were Pteris sensu lato to be divided into smaller genera). Under this definition—a broadly defined Pteris—Pteris is resolved as monophyletic (Fig. 1a) with high support (BS = 100%, PP = 100%, MP JK = 77%—provided that the longbranch attraction artefact was accounted for). With the type Pteris, P. longifolia, included, our analyses are the first to show strong support for the monophyly of the expanded Pteris. The morphological synapomorphies of the newly defined Pteris are rhizome erect or ascending (but long-creeping in Pteris buchananii Sim, Afropteris and Ochropteris), sporangia continuous along commissural veins of pinna margins (but along marginal portions of the veins and not on a commissure in Platyzoma), and pinna apex and pinna base often sterile (but not in Afropteris or Platyzoma, and often not in Ochropteris; acrostichoid in Neurocallis). Placing these genera into Pteris appears to destroy the morphological cohesiveness of Pteris, but apparently, the inconsistent morphological character states in some taxa can most parsimoniously be interpreted as autapomorphic based on our phylogeny (Fig. 1b). above), Platyzoma microphyllum is clearly different from all the other species of Pteris by having two sizes of spores, a dioecious condition of the gametophytes and chromosome number of 2n = 76 (Tryon and Vida, 1967). However, it shares single-pinnate lamina with other members of superclade A (see above). Clade II—the P. grandifolia clade This clade contains only one species, the remarkable P. grandifolia. Plants of the species are large, with leaves 1–4 m, and singly pinnate (rarely with basal pinna pinnate-pinnatifid). Veins of P. grandifolia are copiously anastomosing, the costal areolae are very long, and their long axis is nearly at a right angle to the costa (Fee, 1852). Because of the unusual morphological characters, Fee (1852) proposed a monospecific genus Heterophlebium Fee. Later some authors treated this as a section, Litobrochia sect. Heterophlebia (Fee) T. Moore (Moore, 1857) or P. sect. Heterophlebium (Fee) Hook. (Hooker, 1858; Hooker and Baker, 1874; Christensen, 1906). In Tryon and Tyron’s (1982) six groups of tropical American species of Pteris, it was placed within the “P. haenkeana Group” together with several species that have anastomosing veins and large ultimate pinnae, for example, P. haenkeana C. Presl. Our study provides the first evidence that P. grandifolia is an isolated species, most allied to P. vittata and related species. Morphologically, the two clades share singlepinnate lamina and the terminal pinna larger than the adjacent lateral pinnae. In addition, Copeland (1947) found that the annuli of P. vittata are usually composed of more than 30 thickened cells, a number closer to that of P. grandifolia (26–31) than to those of other species of Pteris (16–20). Major evolutionary lineages of Pteris Clade III—the P. longifolia clade Within the newly defined Pteris (including Afropteris, Neurocallis, Ochropteris and Platyzoma), the 86 species included in the current study are resolved into the following 15 well-supported major clades (Fig. 1b). Most of these major clades are also supported by morphological characters. The 15 major clades listed represent major evolutionary lineages in Pteris at the global level. Before making any taxonomic and nomenclatural decision on infrageneric classification, more samples (especially from the Neotropics, Africa and Malesia) and molecular data (especially nuclear genes) are needed to further test the monophyly of the 15 clades defined. Clade I—the Pteris (Platyzoma) microphylla clade Although the inclusion of Platyzoma in Pteris was strongly supported by our plastid data analysis (see This clade is consistent with the P. longifolia Group determined by Tryon and Tryon (1982). Pteris vittata and P. longifolia were the first species included in Pteris when Linnaeus (1753) published the genus, and the latter is designated as lectotype of Pteris (Smith, 1875). Pteris vittata is one of most widely distributed species in the tropics and subtropics of the Old World, and is commonly naturalized in the New World. Morphologically, P. vittata is similar to P. longifolia; the latter is a polyploid complex that in the broad sense is limited to Mexico and the Caribbean islands (Mickel and Smith, 2004). The two species share nearly the same morphology as a whole, for example, lamina singly pinnate with independent terminal pinna, stipe base densely scaly. Hieronymus (1914) pointed out that P. longifolia has articulate pinna bases and spreading pinnae, which can be used to distinguish it L. Zhang et al. / Cladistics (2014) 1–18 from P. vittata. Our results confirmed the close affinity of the two species, however, the genetic divergence of the two species is distinct (Fig. 1b). The Bahamian endemic P. bahamensis was once treated as a variety of P. longifolia (Hieronymus, 1914), but the former has a glabrous rachis and its pinna bases are never cordate. The sister relationship of the two species is well supported in our analysis. Clade IV—the P. chilensis clade In our sample, this clade contains two species, P. tremula R. Br. and P. chilensis Desv, which were both included in “P. sect. Pteris” by Hooker and Baker (1874) or in the “P. chilensis Group” by Tryon and Tryon (1982). Pteris tremula is distributed in the South Pacific and is often locally naturalized in the Northern Hemisphere. The Chilean endemic P. chilensis is sister to our two P. tremula samples, but the sequence variation between the two species is low. The two species occur naturally far away from each other, but they are consistent morphologically in their threeto four-pinnatifid lamina, ultimate pinnules (lobes) much smaller and veins free. Clade V—the P. semipinnata clade This clade contains only two endemic Asian species —Pteris dimidiata Willd. and P. semipinnata L.—in our sampling. The position of the two species has not been determined in previous classifications (Shieh, 1966; Wu, 1990; Yang, 2011; Liao et al., 2013). Actually, the two species differ from most species of Pteris in having fronds that are singly pinnate, but with the basiscopic side of at least the proximal pinnae pinnatifid or pinnate, but the acroscopic side undivided and poorly developed. Clade VI—the P. longipes clade Species of this clade are endemic to subtropical and tropical Asia. The included four species of this clade were placed in P. sect. Quadriauricula (including P. amoena Blume, P. bella Tagawa and P. longipes D. Don) and P. sect. Campteria (including P. mcclurei Ching) (Liao et al., 2013). None of the previous studies proposed a close affinity among these species. Morphologically, species of this clade have thinner laminae, petioles brown or reddish brown (except P. longipes), and leaves two-pinnate to three-pinnatifid with pectinate pinnae. Pteris longipes differs from other species in this clade in its ternate fronds. Pteris mcclurei has one row of areoles along the costa and was resolved as closely allied to P. amoena, which has free veins. These two species form a well-supported clade. 11 Clade VII—the P. ensiformis clade This clade contains species occurring in America, Asia and Oceania, and encompasses considerable morphological disparity. Our results suggest a close relationship among those species, which has not been suggested by earlier studies due to the lack of diagnostic characters. There are obvious divergences among each species. Two South American species, P. fraseri and P. praestantissimam, together are resolved as monophyletic with strong support. Pteris terminalis Wall. ex J. Agardh (synonym: P. excelsa Gaudich.; Liao et al., 2013) is commonly distributed in Asia, reaching the Hawaiian Islands and Fiji. It is resolved as sister to the monophyletic lineage formed by P. ensiformis and P. insignis Mett. ex Kuhn. Further studies are needed to unravel the evolutionary history of the species in clade VII. Clade VIII—the P. decrescens clade All species of this clade occur in Asia. Our results for the first time disclosed the close relationships among the species in this clade. The morphological circumscription of this clade is difficult; potential diagnostic features include veins free and lamina onepinnate to two-pinnatifid. Three species, P. cadieri, P. decrescens and P. grevilleana, of clade VIII have been observed to have silica bodies on their leaves (Wagner, 1978; Kao et al., 2008; Sundue, 2009). This feature appears to have evolved independently in P. multifida Poir. (clade XV). Three deeply divergent lineages can be recognized within this clade. Forming the first diverging lineage, the Southeast Asian P. heteromorpha Fee and P. pellucida C. Presl are resolved as sister to each other. They together are sister to P. decrescens Christ + a clade containing P. cadieri Christ, P. grevilleana Wall. ex J. Agardh and P. quadristipitis X.Y.Wang & P.S.Wang. Pteris cadieri was resolved as sister to a clade composed of P. grevilleana and P. quadristipitis with maximum support. Except for P. heteromorpha and P. pellucida, all remaining species of clade VIII previously were placed in P. sect. Quadriauricula (Wu, 1990; Liao et al., 2013). Clade IX—the P. quadriaurita clade This clade’s composition is similar to P. sect. Quadriauricula sensu Wu (1990) and Liao et al. (2013). Species of this clade are widespread on four continents. Morphologically they share the lamina two-pinnatifid to two-pinnate, fronds not ternate or pedate, basal pairs of pinnae often with one to three (or four) pinnules near the base on the basiscopic side, and veins free (except P. biaurita L.). Two Asian endemics, P. puberula Ching and P. viridissima Ching, and the 12 L. Zhang et al. / Cladistics (2014) 1–18 Malesian–Australian–South Pacific species P. pacifica Hieron. form the basal grade, followed by an unresolved polytomy. This poorly resolved clade is taxonomically complex and is beyond the scope of the present study. Two samples of P. biaurita from China and Thailand together, respectively, are resolved as sister to the Asian endemic P. griffithii Hook. Two samples of P. linearis Poir. from China and Reunion, respectively, formed a monophyletic clade but sequence divergence between these two samples is pronounced. Our plastid data well resolved the maternal relationships between P. biaurita and P. linearis, while relationships based on morphology seem complicated, as suggested previously by some authors (Walker, 1962; Shieh, 1966). The three African endemics P. catoptera Kunze, P. friesii Hieron. and P. preussii Hieron. form a monophyletic group with the widespread species P. quadriaurita, suggestive of an African origin of the latter. This clade contains one species only, P. dentata Forssk. It formed an unresolved trichotomy with clade XIII and clades XIV + XV. Pteris dentata is widely distributed in the Arabian Peninsula, Sub-Saharan Africa, northwestern Africa and the Mascarenes. This species has the lamina herbaceous and two-pinnate to three-pinnatifid, pinnules (lobes) long and narrow and with toothed distal margins, veins free and lacking anastomosing veins below the sinus. The uncommon morphology and distributional pattern are concordant with the isolated phylogenetic position in the genus (Fig. 1b). Clade X—the P. splendens clade Clade XIII—the P. navarrens clade All species of this clade sampled are distributed in Brazil and were included in Pteris subg. Litobrochia by Christensen (1906). In consideration of the diversity of frond architecture, six species of this clade were included in five groups by Tryon and Tryon (1982). The morphological synapomorphy of this clade could be the anastomosing veins. Except for P. leptophylla Sw., which has only several areolae near costae and costules, all other species in this clade have multiple rows of areolae (Prado and Windisch, 2000). All species of this clade are distributed from Central to South America. The sampled species of this clade largely correspond to Tryon and Tryon’s (1982) Pteris deflexa group when P. propinqua J. Agardh. and P. tripartita are excluded and P. chiapensis A.R. Sm., P. decurrens C. Presl, P. haenkeana and P. speciosa Mett. ex Kuhn are added to the group. This clade can be divided into three subclades. The first subclade contains P. livida Mett. and P. navarrensis Christ, which share large habit, ternate or pedate fronds, and anastomosing veins. The second subclade contains P. decurrens, P. deflexa Link, and P. muricata Hook. The first species has reticulate veins and the other two have free venation. Notably, two samples of P. deflexa did not form a monophyletic clade; more studies on this species are needed. The third subclade contains P. altissima Poir., P. chiapensis, P. haenkeana, P. orizabae M. Martens & Galeotti, P. podophylla Sw. and P. speciosa. The relationships of this subclade are well resolved. Pteris orizabae is sister to the rest of this subclade, followed by P. haenkeana and P. podophylla. Pteris orizabae and P. podophylla both have ternate fronds. The resolution of the morphologically anomalous P. haenkeana in this subclade is surprising. This species has a single pinnate lamina (two pinnate at base), large ultimate pinnae, and is often considered close to P. grandifolia (Tryon and Tryon, 1982; Tryon et al., 1989). Its affinity with P. speciosa was strongly supported. Two samples of P. altissima did not form a monophyletic group because P. chiapensis was placed between the two samples. Generally, species of clade XIII have significant morphological variability: frond pinnate to pedate or ternate, lamina one-pinnate to three- or four-pinnatifid, veins free or anastomosing, Clade XI—the P. tripartita clade All species of this clade are distributed in the Old World (including Oceania) and have large leaves. Some species can grow to 3 m tall, for example, P. arborea L. Except Afropteris barklyae and Ochropteris pallens, all other species have anastomosing veins. This clade can be divided into four subclades. The first contains P. arborea, P. finotii Christ, P. tripartita Sw. and P. wallichiana J. Agardh.; species of this subclade have largely pedate fronds. The Old World widespread tropical species P. tripartite, together with P. arborea, is sister to the Asian endemic P. finotii plus P. wallichiana. The second subclade contains only the African endemic P. buchananii. The third subclade contains Afropteris barklyae and Ochropteris pallens, two endemics of Indian Ocean islands, all with free veins. The morphology of the sporangia of both is similar to that of Pteris. The fourth subclade contains four Oceanian species, P. comans G. Forst., P. macilenta A. Rich., P. microptera Mett. ex Kuhn and P. saxatilis Carse, all with anastomosing veins. These four species are similar to one another in morphology and thus are sometimes treated as a complex (Bostock et al., 1998). Our data resolved the Lord Howe Island endemic P. microptera as sister to a clade of the remaining three taxa. Clade XII—the P. dentata clade L. Zhang et al. / Cladistics (2014) 1–18 etc. However, most species of this clade have toothed distal pinna margins and anastomosing veins (except P. deflexa and P. muricata). Clade XIV—the P. mutilata clade This clade contains five species, P. burtonii Baker, P. commutata Kuhn, P. mutilata L., P. pungens Willd. and P. usambarensis Hieron., and can be divided into two well-supported subclades. Two American endemics, P. mutilata and P. pungens, constitute the first subclade. Pteris pungens is a relatively common species ranging from Mesoamerica to South America. It is morphologically similar to members of the P. quadriaurita complex and was placed in the “P. quadriaurita Group” by Tryon and Tryon (1982). However, this species has one or two veinlets arising from the costa between adjacent ultimate segments, as well as reddish brown stipe with sparse spines and often much longer than the lamina, making it distinct from other species of the “P. quadriaurita Group”. Pteris mutilata is one of eight taxa first recognized by Linnaeus (1753) in the genus Pteris and is distributed only in parts of the Caribbean. This species has dimorphic fronds, single-pinnate lamina and basal pinnae often pinnate or pinnatifid, which is similar to P. ensiformis, but P. mutilata has slender cartilaginous margins of the sterile pinnules (Hooker, 1858). The close phylogenetic relationship between P. mutilata and P. pungens is unexpected given their morphological differences. Three African endemics form the second subclade. The sympatric P. burtonii and P. commutata are closely related and share sessile and decurrent pinnae. The two species together are sister to P. usambarensis with strong support values. The latter grows in Kenya and Tanzania and differs from other species of this clade in having distinct stalks on the lower pinnae. Clade XV—the P. cretica clade This clade largely corresponds to Pteris sect. Pteris sensu Wu (1990) and Liao et al. (2013). All species of this clade are native to the Old World (P. cretica L. and P. multifida are possibly naturalized in the New World). This clade is characterized by having dimorphic fronds and often singly pinnate and veins free. Three well-supported subclades can be identified. The first subclade is represented by the widespread P. cretica and some regional endemics. The Australian endemic P. umbrosa is resolved as sister to a clade composed of P. cretica, P. japonica Mett., P. multifida and P. nanlingensis R. H. Miau, all of which except P. cretica occur only in eastern Southeast Asia. The second subclade contains three southern Chinese– Southeast Asian species P. morii Masam., P. pseudopellucida Ching and an undetermined Indonesian spe- 13 cies. The third subclade contains eight species mostly distributed in limestone areas: P. actiniopteroides Christ, P. dactylina Hook., P. gallinopes Ching, P. henryi Christ, P. multifida, P. deltodon Baker and P. xiaoyingiae H. He & Li Bing Zhang. The latter two (P. deltodon and P. xiaoyingiae) together are strongly supported as sister to a clade containing the other seven species. Interestingly, these two have ovate to elliptic pinnae, whereas the other seven have linear to lanceolate pinnae. Pteris multifida has conspicuously decurrent pinnae. Pteris deltodon and P. xiaoyingiae often occur on limestone cliffs and the close relationship between them has been recognized morphologically (He and Zhang, 2010) as well as with molecular data (Fig. 1b). 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BMC Evol. Biol. 12, 180. Zhang, L., Zhou, X.-M., Gao, X.-F., Zhang, L.-B., 2014. Pteris barklyae (Pteridaceae): a new combination and lectotypication of Adiantum pallens for the fern flora of the Indian Ocean Islands. Phytotaxa, 174, 116–118. Zurawski, G., Clegg, M.T., Brown, A.H.D., 1984. The nature of nucleotide sequence divergence between barley and maize chloroplast DNA. Genetics 106, 735–749. Appendix 1 Holmgren and Holmgren (1998), list of taxa sampled with information related to taxonomy, and GenBank accession numbers. Herbarium acronyms follow Index Herbariorum (Holmgren and Holmgren, 1998). Acrostichum danaeifolium Langsd. & Fisch., E. Schuettpelz 616 (B): rbcL EF452129 (Schuettpelz et al., 2007), atpB EF452008 (Schuettpelz et al., 2007), atpA EF452065 (Schuettpelz et al., 2007); 1003W (cult.): rbcL KM008126, atpB KM007673, atpA KM007556, rps4-trnS KM007785. 16 L. Zhang et al. / Cladistics (2014) 1–18 Actiniopteris dimorpha Pic. Serm., Schneider s.n. (GOET): rbcL EF452130 (Schuettpelz et al., 2007), atpB EF452009 (Schuettpelz et al., 2007), atpA EF452066 (Schuettpelz et al., 2007), trnL KM008014, trnL-F KM007902, rps4-trnS KM007786. Actiniopteris semiflabellata Pic. Serm., Smith s.n. (UC): rbcL KM008127, atpB KM007674, atpA KM007557, trnL KM008015, trnL-F KM007903, rps4-trnS KM007787. Adiantum capillusveneris L., Wen 10360 (US): rbcL JF935345 (Lu et al., 2012), atpB JF935427 (Lu et al., 2012), atpA JF937300 (Lu et al., 2012). Anogramma guatemalensis (Domin) C. Chr., Gastony 1037D (IND) & Smith 2586 (UC): rbcL AY168716 (Nakazato and Gastony, 2003), rps4-trnS AF321699 (Sanchez-Baracaldo, 2004a). Anogramma leptophylla (L.) Link, Zylinski s.n. (DUKE): rbcL KM008128, atpB KM007675, atpA KM007558, trnL KM008016, trnL-F KM007904, rps4-trnS KM007788. Austrogramme decipiens (Mett.) Hennipman, H. van der Werff 16114 (UC): rps4-trnS AF321702 (Sanchez-Baracaldo, 2004a). Austrogramme marginata (Mett.) E. Fourn., D. Hodel 1454 (UC): rps4-trnS AY357704 (Sanchez-Baracaldo, 2004a). Ceratopteris richardii Brongn., Killip 44595(GH): rbcL EU352297 (Rai and Graham, 2010), atpB AY612691 (Pryer et al., 2004), atpA DQ390550 (Schuettpelz et al., 2006), rps4-trnS AY612653 (Pryer et al., 2004). Cerosora microphylla (Hook.) R.M. Tryon, Jin 11264 (CDBI): atpB KM007676, atpA KM007559, rps4-trnS KM007789. Cosentinia vellea (Aiton) Tod., Larsson 55 (UPS, DUKE): rbcL KM008129, atpB KM007677, atpA KM007560, trnL KM008017, trnL-F KM007905, rps4-trnS KM007790. Eriosorus cheilanthoides (Sw.) A.F. Tryon, Moran 7579 (NY): rbcL EF452152 (Schuettpelz et al., 2007), atpB EF452034 (Schuettpelz et al., 2007), atpA EF452095 (Schuettpelz et al., 2007). Eriosorus elongatus (Grev. & Hook.) Copel., Rothfels 3602 (DUKE): rbcL KM008130, atpB KM007678, atpA KM007561, trnL KM008018, trnL-F KM007906, rps4-trnS KM007791. Eriosorus flexuosus (Kunth) Copel., Rothfels 08-042 (DUKE): rbcL KM008132, atpB KM007680, atpA KM007562, trnL KM008019, trnL-F KM007908, rps4-trnS KM007793; Rothfels et al. 3552 (DUKE): rbcL KM008131, atpB KM007679, atpA KM007563, trnL KM008020, trnL-F KM007907, rps4-trnS KM007792. Eriosorus hirtus (Kunth) Copel., Rothfels 3668 (DUKE): rbcL KM008133, atpB KM007681, atpA KM007564, trnL KM008021, trnL-F KM007909, rps4-trnS KM007794. Jamesonia goudotii (Hieron.) C. Chr., Rothfels 3694 (DUKE): rbcL KM008134, atpB KM007682, atpA KM007565, trnL KM008022, trnL-F KM007910, rps4-trnS KM007795. Jamesonia scammaniae A.F. Tryon, Rothfels 2631 (DUKE): rbcL KM008135, atpB KM007683, atpA KM007566, trnL KM008023, trnL-F KM007911, rps4-trnS KM007796. Jamesonia verticalis Kunze, Moran 7593 (NY): rbcL EF452155 (Schuettpelz et al., 2007), atpB EF452038 (Schuettpelz et al., 2007), atpA EF452099 (Schuettpelz et al., 2007); Rothfels 3638 (DUKE): rbcL KM008136, atpB KM007684, atpA KM007567, trnL KM008024, trnL-F KM007912, rps4-trnS KM007797. Onychium contiguum Wall. ex C. Hope, Gao 13378 (CDBI): rbcL KM008137, atpB KM007685, atpA KM007568, trnL KM008025, trnL-F KM007913, rps4-trnS KM007798. Onychium japonicum (Thunb.) Kunze, Zhang et al. 5997 (CDBI): rbcL KM008138, atpB KM007686, atpA KM007569, trnL KM008026, trnL-F KM007914, rps4-trnS KM007799. Pityrogramma austroamericana Domin, E. Schuettpelz 301 (DUKE): rbcL EF452166 (Schuettpelz et al., 2007), atpB EF452050 (Schuettpelz et al., 2007), atpA EF452112 (Schuettpelz et al., 2007), rps4-trnS AF321698 (Schuettpelz et al., 2007). Pityrogramma calomelanos (L.) Link, Rothfels et al. 08-107 (DUKE): rbcL KM008139, atpB KM007687, atpA KM007570, trnL KM008027, trnL-F KM007915, rps4-trnS KM007800; Zhang Liang 1186 (CDBI): rbcL KM008140, atpB KM007688, atpA KM007571, trnL KM008028, trnL-F KM007916, rps4-trnS KM007801. Pityrogramma ebenea (L.) Proctor, Rothfels et al. 08-19 (DUKE): rbcL KM008141, atpB KM007689, atpA KM007572, rps4-trnS KM007802. Pityrogramma jamesonii (Baker) Domin, Moran 7592 (NY): rbcL EF452167 (Schuettpelz et al., 2007), atpB EF463519 (Schuettpelz et al., 2007), atpA EF463857 (Schuettpelz et al., 2007). Pityrogramma ochracea (C. Presl) Domin, Araujo 4253 (MO): rbcL KM008142, atpB KM007690, atpA KM007573, trnL KM008029, trnL-F KM007917, rps4-trnS KM007803. Pityrogramma presliana Domin, Rothfels et al. 3664 (DUKE): rbcL KM008143, atpB KM007691, atpA KM007574, trnL KM008030, trnL-F KM007918, rps4-trnS KM007804. Pityrogramma trifoliata (L.) R.M. Tryon, Rothfels 3658 (DUKE): rbcL KM008145, atpB KM007693, atpA KM007576, trnL KM008032, trnL-F KM007920, rps4-trnS KM007806. Pityrogramma sp., Rothfels 3608 (DUKE): rbcL KM008144, atpB KM007692, atpA KM007575, trnL KM008031, trnL-F KM007919, rps4-trnS KM007805. Platyzoma microphyllum R. Br., Bostock s.n. (IND): rbcL AY168721 (Nakazato and Gastony, 2003), atpB KM007694, atpA KM007577, trnL KM008033, trnL-F KM007921, rps4-trnS KM007811. Pteris actiniopteroides Christ, Zhang Liang 1384 (CDBI): rbcL KM008146, atpB KM007696, atpA KM007580, trnL KM008036, trnL-F KM007924, rps4-trnS KM007812. Pteris altissima Poir., 1002w (cult.): atpB KM007697, atpA KM007581, trnL KM008037, trnL-F KM007925, rps4-trnS KM007813; Nitta 863 (UC): rbcL KM008147, atpB KM007698, atpA KM007582, trnL KM008038, trnL-F KM007926. Pteris amoena Blume, Qingzang 74-5078 (KUN): rbcL KM008148, atpA KM007583, trnL KM008039, trnLF KM007927, rps4-trnS KM007814. Pteris arborea L., Christenhusz 4050 (TUR): rbcL KM008149, atpB KM007699, atpA KM007584. Pteris bahamensis (J. Agardh) Fee, Rothfels 4024 (DUKE): rbcL KM008150, atpB KM007700, atpA KM007585, trnL KM008040, trnL-F KM007928, rps4-trnS KM007815. Pteris barklyae “Afropteris barklyae (Baker) Alston”, Kramer 11086 (Z): rps4-trnS AF544984 (Sanchez-Baracaldo, 2004b). Pteris bella Tagawa, Wu s.n. (KUN): rbcL KM008151, atpB KM007701, atpA KM007586, trnL KM008041, trnL-F KM007929, rps4-trnS KM007816; Zhang Liang 1300 (CDBI): rbcL KM008152, atpB KM007702, atpA KM007587, trnL KM008042, trnL-F KM007930, rps4-trnS KM007817. Pteris biaurita L., Larsen 44455 (MO): rbcL KM008153, atpB KM007703, atpA KM007588, trnL KM008043, trnL-F KM007931, rps4-trnS KM007818; Zhang Liang 1310 (CDBI): rbcL KM008154, atpB KM007704, atpA KM007589, trnL KM008044, trnL-F KM007932, rps4-trnS KM007819. Pteris brasiliensis Raddi, Prado 2049 (SP): rbcL KM008155, atpB KM007705, atpA KM007590, trnL KM008045, trnL-F KM007933, rps4-trnS KM007820. Pteris buchananii Sim, Kamau 382 (EA): rbcL KM008156, atpB KM007706, atpA KM007591, trnL KM008046, trnL-F KM007934, rps4-trnS KM007821. Pteris burtonii Baker, Kamau 227 (EA): rbcL KM008157, atpB KM007707, atpA KM007592, trnL KM008047, trnL-F KM007935, rps4-trnS KM007822. Pteris cadieri Christ, Zhang Liang 1240 (CDBI): rbcL KM008158, atpB KM007708, atpA KM007593, trnL KM008048, trnL-F KM007936, rps4-trnS KM007823. Pteris catoptera Kunze, Kamau 463 (EA): rbcL KM008159, atpB KM007709, atpA KM007594, trnL KM008049, rps4-trnS KM007824. Pteris chiapensis A.R. Sm., P erez-Farrera 2978 (MO): rbcL KM008160, atpB KM007710, atpA KM007595, trnL KM008050, trnL-F KM007937, rps4-trnS KM007825. Pteris chilensis Desv., Z€ ollner 17416 (MO): rbcL KM008161, atpB KM007711, atpA KM007596, trnL KM008051, trnL-F KM007938, rps4-trnS KM007826. Pteris comans G. Forst., Welt P20796 (WELT): rbcL EF469954, atpB GU136777. Pteris commutata Kuhn, Kamau 331 (EA): rbcL KM008162, atpB KM007712, atpA KM007597, trnL KM008052, L. Zhang et al. / Cladistics (2014) 1–18 trnL-F KM007939, rps4-trnS KM007827. Pteris cretica L., Jin 11016 (CDBI): rbcL KM008163, atpB KM007713, atpA KM007598, trnL KM008053, trnL-F KM007940, rps4-trnS KM007828. Pteris dactylina Hook., Zhang Liang 1391 (CDBI): rbcL KM008164, atpB KM007714, atpA KM007599, trnL KM008054, trnL-F KM007941, rps4-trnS KM007829. Pteris decrescens Christ, Pan 053 (GZTM): rbcL KM008166, atpB KM007716, atpA KM007601, trnL KM008056, trnL-F KM007943, rps4-trnS KM007831; Zhang et al. 5474 (CDBI): rbcL KM008165, atpB KM007715, atpA KM007600, trnL KM008055, trnL-F KM007942, rps4-trnS KM007830. Pteris decurrens C. Presl, Prado 1082 (SP): rbcL EF473703 (Prado et al., 2007). Pteris deflexa Link, Prado 1089 (SP): rbcL EF473704 (Prado et al., 2007); Prado 2124 (SP): rbcL KM008167, atpB KM007717, atpA KM007602, trnL KM008057, trnL-F KM007944, rps4-trnS KM007832. Pteris deltodon Baker, Zhang Liang 1356 (CDBI): rbcL KM008168, atpB KM007718, atpA KM007603, trnL KM008058, trnL-F KM007945 rps4-trnS KM007833. Pteris dentata Forssk., Tamon s.n.: rbcL KM008169, atpB KM007719, atpA KM007604, trnL KM008059, trnL-F KM007946, rps4-trnS KM007834. Pteris denticulata Sw., Prado 2159 (SP): rbcL KM008170, atpB KM007720, atpA KM007605, trnL KM008060, trnL-F KM007947, rps4-trnS KM007835; Prado 1084 (SP): rbcL EF473705. Pteris dimidiata Willd., E. Schuettpelz 893 (DUKE): rbcL KM008171, atpB KM007721, atpA KM007606, trnL KM008061, trnL-F KM007948, rps4-trnS KM007836; Zhang Liang 1287 (CDBI): rbcL KM008172, atpB KM007722, atpA KM007607, trnL KM008062, trnL-F KM007949, rps4-trnS KM007837. Pteris ensiformis Burm., ARF3539 (cult.): rbcL KM008173, atpB KM007723, atpA KM007608, trnL KM008063, trnL-F KM007950, rps4-trnS KM007838; Zhang Liang 1312 (CDBI): rbcL KM008174, atpB KM007724, atpA KM007609, trnL KM008064, trnL-F KM007951, rps4-trnS KM007839. Pteris esquirolii Christ, Pan 033 (GZTM): rbcL KM008175, atpB KM007725, atpA KM007610, trnL KM008065, trnL-F KM007952, rps4-trnS KM007840. Pteris finotii Christ, Zhang Liang 1323 (CDBI): rbcL KM008176, atpB KM007726, atpA KM007611, trnL KM008066, trnL-F KM007953, rps4-trnS KM007841. Pteris fraseri Mett. ex Kuhn, Rothfels 3712 (DUKE): rbcL KM008177, atpB KM007727, atpA KM007612, trnL KM008067, trnL-F KM007954, rps4-trnS KM007842. Pteris friesii Hieron., Festo & Kayombo 430 (MO): rbcL KM008178, atpA KM007613, trnL KM008068, trnL-F KM007955, rps4-trnS KM007843. Pteris gallinopes Ching, He 1378 (CTC): rbcL KM008179, atpB KM007728, atpA KM007614, trnL KM008069, trnL-F KM007956, rps4-trnS KM007844. Pteris grandifolia L., Rodas 296 (MO): rbcL KM008180, atpB KM007729, atpA KM007615, trnL KM008070, trnL-F KM007957, rps4-trnS KM007845. Pteris grevilleana Wall. ex J. Agardh, Zhang Liang 1319 (CDBI): rbcL KM008181, atpB KM007730, atpA KM007616, trnL KM008071, trnL-F KM007958, rps4-trnS KM007846. Pteris griffithii Hook., Deng 3818 (CDBI): rbcL KM008182, atpB KM007731, atpA KM007617, trnL KM008072, trnL-F KM007959, rps4-trnS KM007847. Pteris haenkeana C. Presl, H. van der Werff 17869 (MO): rbcL KM008183, atpB KM007732, atpA KM007618, trnL KM008073, trnL-F KM007960, rps4-trnS KM007848. Pteris henryi Christ, Zhang et al. 6038 (CDBI): rbcL KM008184, atpB KM007733, atpA KM007619, trnL KM008074, trnL-F KM007961, rps4-trnS KM007849. Pteris heteromorpha Fee, Wu ws-2622 (MO): rbcL KM008185, atpB KM007734, atpA KM007620, trnL KM008075, trnL-F KM007962, rps4-trnS KM007850. Pteris insignis Mett. ex Kuhn, Zhang Liang 1274 (CDBI): rbcL KM008186, atpB KM007735, atpA KM007621, trnL KM008076, trnL-F KM007963, rps4-trnS KM007851. 17 Pteris japonica (Thunb.) Mett., E. Schuettpelz 1070 (DUKE): rbcL KM008187, atpB KM007736, atpA KM007622, trnL KM008077, trnL-F KM007964, rps4-trnS KM007852. Pteris lechleri Mett., Prado 2061 (SP): rbcL KM008188, atpB KM007737, atpA KM007623, trnL KM008078, trnL-F KM007965, rps4-trnS KM007853; Prado 2190 (SP): rbcL KM008189, trnL KM008079, trnL-F KM007966, rps4-trnS KM007854. Pteris leptophylla Sw., Boldrin 160 (SP): rbcL EF473707 (Prado et al., 2007). Pteris linearis Poir., Grangaud s.n. (MO): rbcL KM008190, atpB KM007738, atpA KM007624, trnL KM008080, trnL-F KM007967, rps4-trnS KM007855; Zhang Liang 1309 (CDBI): rbcL KM008191, atpB KM007739, atpA KM007625, trnL KM008081, trnL-F KM007968, rps4-trnS KM007856. Pteris livida Mett., E. Schuettpelz 936 (DUKE): rbcL KM008192, atpB KM007740, atpA KM007626, trnL KM008082, trnL-F KM007969, rps4-trnS KM007857. Pteris longifolia L., Rothfels 3276 (DUKE): rbcL KM008193, atpB KM007741, atpA KM007627, trnL KM008083, trnL-F KM007970, rps4-trnS KM007858. Pteris longipes D. Don, Jin 11507 (CDBI): rbcL KM008194, atpB KM007742, atpA KM007628, trnL KM008084, trnL-F KM007971, rps4-trnS KM007859; Zhang Liang 1321 (CDBI): rbcL KM008195, atpB KM007743, atpA KM007629, trnL KM008085, trnL-F KM007972, rps4-trnS KM007860. Pteris macilenta A. Rich., Welt P021006 (WELT): rbcL GU136797 (Bouma et al., 2010), atpB GU136778 (Bouma et al., 2010). Pteris mcclurei Ching, Zhang Liang 1289 (CDBI): rbcL KM008196, atpB KM007744, atpA KM007630, trnL KM008086, trnL-F KM007973, rps4-trnS KM007861. Pteris microptera Mett. ex Kuhn, Papadopulos AP960: rbcL JF950814 (Papadopulos et al., 2011). Pteris morii Masam., Zhang Liang 1314 (CDBI): rbcL KM008197, atpB KM007745, atpA KM007631, trnL KM008087, trnL-F KM007974 rps4-trnS KM007862; Zhang Liang 1328 (CDBI): rbcL KM008198, atpB KM007746, atpA KM007632, trnL KM008088, trnL-F KM007975, rps4-trnS KM007863. Pteris multifida Poir., Rothfels 3960 (DUKE): rbcL KM008199, atpB KM007747, atpA KM007633, trnL KM008089, trnL-F KM007976, rps4-trnS KM007864; E. Schuettpelz 710 (DUKE): rbcL KM008229, atpB KM007776, atpA KM007663, trnL KM008117, trnL-F KM008005, rps4-trnS KM007894; Zhang Liang 1167 (CDBI): rbcL KM008200, atpB KM007748, atpA KM007634, trnL KM008090, trnL-F KM007977, rps4-trnS KM007865. Pteris muricata Hook., Rothfels 3745 (DUKE): rbcL KM008201, atpB KM007749, atpA KM007635, trnL KM008091, trnL-F KM007978, rps4-trnS KM007866. Pteris mutilata L., Sundue 2096 (MO): rbcL KM008202, atpB KM007750, atpA KM007636, trnL KM008092, trnL-F KM007979, rps4-trnS KM007867. Pteris nanlingensis R. H. Miau, Zhang et al. 6003 (CDBI): rbcL KM008203, atpB KM007751, atpA KM007637, trnL KM008093, trnL-F KM007980, rps4-trnS KM007868. Pteris navarrensis Christ, Rothfels 2640 (DUKE): rbcL KM008204, atpB KM007752, atpA KM007638, trnL KM008094, trnL-F KM007981, rps4-trnS KM007869. Pteris orizabae M. Martens & Galeotti, Reyes-Garcıa 7311 (MO): rbcL KM008205, atpB KM007753, atpA KM007639, trnL-F KM007982, rps4-trnS KM007870. Pteris pacifica Hieron., ARF3536 (cult.): rbcL KM008206, atpB KM007754, atpA KM007640, trnL KM008095, trnL-F KM007983, rps4-trnS KM007871. Pteris pallens (Sw.) Mett., Janssen 2677 (P): rbcL KM008207, atpB KM007755, atpA KM007641, trnL KM008096, trnL-F KM007984, rps4-trnS KM007872. Pteris pellucida C. Presl, Xia 172 (CDBI): rbcL KM008208, atpB KM007756, atpA KM007642, trnL KM008097, trnL-F KM007985, rps4-trnS KM007873. Pteris podophylla Sw., Rothfels 3746 (DUKE): rbcL KM008209, atpB KM007757, atpA KM007643, trnL KM008098, trnL-F KM007986, rps4-trnS KM007874. Pteris praestantissima (Bory ex Fee) Christenh., Rothfels 2680 (DUKE): rbcL 18 L. Zhang et al. / Cladistics (2014) 1–18 KM008210, atpB KM007758, atpA KM007644, trnL KM008099, trnL-F KM007987, rps4-trnS KM007875; Christenhusz 3997 (TUR): rbcL EF452158 (Schuettpelz et al., 2007), atpB EF452042 (Schuettpelz et al., 2007), atpA EF452104 (Schuettpelz et al., 2007). Pteris preussii Hieron., Kamau 212 (EA): rbcL KM008211, atpB KM007759, atpA KM007645, rps4-trnS KM007876. Pteris propinqua J.Agardh, E. Schuettpelz 268 (DUKE): rbcL KM008212, atpB KM007760, atpA KM007646, trnL KM008100, trnL-F KM007988, rps4-trnS KM007877. Pteris pseudopellucida Ching, Wu ws-2580 (MO): rbcL KM008213, atpB KM007761, atpA KM007647, trnL KM008101, trnL-F KM007989, rps4-trnS KM007878. Pteris puberula Ching, Jin 11305 (CDBI): rbcL KM008214, atpB KM007762, atpA KM007648, trnL KM008102, trnL-F KM007990, rps4-trnS KM007879. Pteris pungens Willd., Rothfels 08-165 (DUKE): rbcL KM008215, atpB KM007763, atpA KM007649, trnL KM008103, trnL-F KM007991, rps4-trnS KM007880. Pteris quadriaurita Retz., E. Schuettpelz 546 (GOET): rbcL EF452173 (Schuettpelz et al., 2007), atpB EF452058 (Schuettpelz et al., 2007), atpA EF452121 (Schuettpelz et al., 2007). Pteris quadristipitis X.Y. Wang & P.S. Wang, Sun s.n. (CDBI): rbcL KM008216, atpB KM007764, atpA KM007650, trnL KM008104, trnL-F KM007992, rps4-trnS KM007881. Pteris saxatilis Carse, Welt P022567 (WELT): rbcL GU136798 (Bouma et al., 2010), atpB GU136779 (Bouma et al., 2010). Pteris semipinnata L., Zhang Liang 1463 (CDBI): rbcL KM008217, atpB KM007765, atpA KM007651, trnL KM008105, trnL-F KM007993, rps4-trnS KM007882. Pteris setulosocostulata Hayata, Zhang Liang 1379 (CDBI): rbcL KM008218, atpB KM007766, atpA KM007652, trnL KM008106, trnL-F KM007994, rps4-trnS KM007883. Pteris speciosa Mett. ex Kuhn, Nitta 777 (UC): rbcL KM008219, atpB KM007767, atpA KM007653, trnL KM008107, trnL-F KM007995, rps4-trnS KM007884. Pteris splendens Kaulf., Prado 1131a: rbcL EF473708 (Prado et al., 2007). Pteris splendida Ching, Zhang et al. 5632 (CDBI): rbcL KM008220, atpB KM007768, atpA KM007654, trnL KM008108, trnL-F KM007996, rps4-trnS KM007885. Pteris terminalis Wall. ex J. Agardh, Zhang Liang 1341 (CDBI): rbcL KM008221, atpB KM007769, atpA KM007655, trnL KM008109, trnL-F KM007997, rps4-trnS KM007886. Pteris tremula R. Br., ARF3535 (cult.): rbcL KM008222, atpB KM007770, atpA KM007656, trnL KM008110, trnL-F KM007998, rps4-trnS KM007887; E. Schuettpelz 620 (B): rbcL KM008223, atpB KM007771, atpA KM007657, trnL KM008111, trnL-F KM007999, rps4-trnS KM007888. Pteris tripartita Sw., ARF3538 (cult.): rbcL KM008224, atpB KM007772, atpA KM007658, trnL KM008112, trnL-F KM008000, rps4-trnS KM007889; E. Schuettpelz 621(B): rbcL KM008225, atpB KM007773, atpA KM007659, trnL KM008113, trnL-F KM008001, rps4-trnS KM007890. Pteris umbrosa R. Br., ARF3537 (cult.): rbcL KM008226, atpB KM007774, atpA KM007660, trnL KM008114, trnL-F KM008002, rps4-trnS KM007891; Field s.n. (BRI): rbcL KM008227, atpA KM007661, trnL KM008115, trnL-F KM008003, rps4-trnS KM007892. Pteris usambarensis Hieron., Kamau 388 (EA): rbcL KM008228, atpB KM007775, atpA KM007662, trnL KM008116, trnL-F KM008004, rps4-trnS KM007893. Pteris viridissima Ching, Zhang & He 5944 (CDBI): rbcL KM008230, atpB KM007777, atpA KM007664, trnL KM008118, trnL-F KM008006, rps4-trnS KM007895. Pteris vittata L., ARF3534 (cult.): rbcL KM008231, atpB KM007778, atpA KM007665, trnL KM008119, trnL-F KM008007, rps4-trnS KM007896; Rothfels 4016 (DUKE): rbcL KM008232, atpB KM007779, atpA KM007666, trnL KM008120, trnL-F KM008008, rps4-trnS KM007897; Zhang Liang 1466 (CDBI): rbcL KM008233, atpB KM007780, atpA KM007667, trnL KM008121, trnL-F KM008009, rps4-trnS KM007898. Pteris wallichiana J. Agardh, Zhang Liang 1284 (CDBI): rbcL KM008235, atpB KM007782, atpA KM007669, trnL KM008123, trnL-F KM008011, rps4-trnS KM007900. Pteris wallichiana var. yunnanensis (Christ) Ching & S.H. Wu, Jin 11183 (CDBI): rbcL KM008234, atpB KM007781, atpA KM007668, trnL KM008122, trnL-F KM008010, rps4-trnS KM007899. Pteris xiaoyingiae H. He & Li Bing Zhang, Zhang & He 5326 (CDBI): rbcL KM008236, atpB KM007783, atpA KM007670, trnL KM008124, trnL-F KM008012, rps4-trnS KM007901. Pteris sp., Wen 10179 (US): rbcL JF935342 (Lu et al., 2012), atpB JF935424 (Lu et al., 2012), atpA JF937297 (Lu et al., 2012), trnL-F JF980687 (Lu et al., 2012), rps4-trnS JF980608 (Lu et al., 2012). Pterozonium brevifrons (A.C.Sm.) Lellinger, E. Schuettpelz 285 (DUKE): rbcL EF452175 (Schuettpelz et al., 2007), atpB EF452061 (Schuettpelz et al., 2007), atpA EF452124 (Schuettpelz et al., 2007); Neill 15671 (MO): rbcL KM008237, atpA KM007578, trnL KM008034, trnL-F KM007922, rps4-trnS KM007807. Pterozonium reniforme (Mart.) Fee, van der Werff 16216 (MO): rbcL KM008238, atpB KM007695, atpA KM007579, trnL KM008035, trnL-F KM007923, rps4-trnS KM007808. Syngramma quinata (Hook.) Carruth., M. Kessler 2273 (L): rps4trnS AF321701 (Sanchez-Baracaldo, 2004a). Taenitis blechnoides (Willd.) Sw., E. Schuettpelz 689 (DUKE): rbcL KM008239, atpB KM007784, atpA KM007671, trnL KM008125, trnL-F KM008013 rps4-trnS KM007809. Taenitis interrupta Hook. & Grev., E. Schuettpelz 851 (DUKE): rbcL KM008240, atpA KM007672, rps4-trnS KM007810. Tryonia myriophylla (Sw.) Schuettp., Prado & Yano 1033 (SP): rbcL EF473710 (Prado et al., 2007); Prado 896: rps4-trnS AF321706 (Sanchez-Baracaldo, 2004a); Prado 999: rps4-trnS AF321707 (Sanchez-Baracaldo, 2004a).

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A global plastid phylogeny of the brake fern genus Pteris (Pteridaceae) and related genera in the Pteridoideae

A global plastid phylogeny of the brake fern genus Pteris (Pteridaceae) and related genera in the Pteridoideae

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