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Molecular Phylogeny of the Fern Genus Elaphoglossum

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Molecular Phylogeny of the Fern Genus Elaphoglossum MOLECULAR PHYLOGENETICS AND EVOLUTION Molecular Phylogenetics and Evolution 33 (2004) 745–763 www.elsevier.com/locate/ympev Molecular phylogeny of the fern genus Elaphoglossum (Elaphoglossaceae) based on chloroplast non-coding DNA sequences: contributions of species from the Indian Ocean area Germinal Rouhana,b,*, Jean-Yves Dubuissonb, France Rakotondrainibea,c, Timothy J. Motleyd, John T. Mickele, Jean-Noe¨l Labata, Robbin C. Morane a De´partement Syste´matique et Evolution USM 602, Herbier National Plantes Vasculaires, Muse´um National dÕHistoire Naturelle, 16 rue Buffon, 75005 Paris, France b Equipe ‘‘Classification, Evolution et Biosyste´matique’’ (EA 3496) Laboratoire de Pale´obotanique et Pale´oe´cologie, UMR 5143, Universite´ Pierre et Marie Curie, 12 rue Cuvier, 75005 Paris, France c Laboratoire de Biologie et Evolution des Plantes vasculaires, Ecole Pratique des Hautes Etudes, Muse´um National dÕHistoire Naturelle, 16 rue Buffon, 75005 Paris, France d The Lewis B. and Dorothy Cullman Program for Molecular Systematics Studies, The New York Botanical Garden, Bronx, NY 10458-5126, USA e New York Botanical Garden, Bronx, NY 10458-5126, USA Received 9 February 2004; revised 12 May 2004 Available online 25 September 2004 Abstract We performed a phylogenetic analysis of the fern genus Elaphoglossum using two non-coding chloroplast spacers: trnL-trnF and rps4-trnS. The sampling includes 123 species, of which 80 have not been previously sequenced, and for the first time includes species from Africa and the Indian Ocean area. The results of this expanded study largely agree with an earlier molecular study based on a smaller group of neotropical species and with the morphology-based classification of Mickel and Atehortu´a. We found, however, that some infrageneric groups such as section Elaphoglossum are not monophyletic. Besides section Elaphoglossum pro parte, we recognize six sections: two new monospecific, unnamed sections, and the previously established sections Lepidoglossa, Squamipedia, Amygdal- ifolia, and ‘‘Subulate-scaled clade.’’ We divide the subulate-scaled clade into subsection Setosa (hydathodes present) and Polytrichia (hydathodes absent), and section Elaphoglossum is divided into subsections Platyglossa and Pachyglossa, two groups that do not appear to be supported by any single morphological character. In general, however, the main clades are supported by morphology. Finally, we discuss the species of the Indian Ocean region and their affinities with the neotropical ones. Out of the 11 species pairs postulated by Moran and Smith on the basis of morphology, two are well supported (E. eximium–E. aubertii; E. piloselloides–E. spatulatum) and three are not supported (E. ciliatum–E. humbertii; E. muscosum–E. poolii; E. paleaceum–E. deckenii), and two remain unresolved (E. erinaceum–E. hybridum; E. glabellum–E. acrostichoides) because our molecular markers were not variable enough. Four species pairs could not be tested because specimens were lacking. Unsupported species pairs are best interpreted as morphological convergences. Two additional species pairs are proposed: E. cuspidatum–E. succisaefolium; E. doanense–E. hornei. Placement of the species from the Indian Ocean suggests that at least 13 long-distance dispersal events occurred between the Neo- tropics and the Indian Ocean-Africa. Ó 2004 Elsevier Inc. All rights reserved. Keywords: Elaphoglossum; Elaphoglossaceae; Ferns; Lomariopsidaceae; trnL-trnF; rps4-trnS; Phylogeny; Systematics; Indian Ocean; Biogeography; Islands * Corresponding author. Fax: +33 1 40 79 33 42. E-mail address: [email protected] (G. Rouhan). 1055-7903/$ - see front matter Ó 2004 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2004.08.006 746 G. Rouhan et al. / Molecular Phylogenetics and Evolution 33 (2004) 745–763 1. Introduction trnF, and rps4-trnS (Skog et al., 2004). This work con- cluded that Elaphoglossum was monophyletic and, Elaphoglossum (Elaphoglossaceae) is one of the most among the outgroups they used, sister to Bolbitis. With- diversified fern genera, with over 600 species. These in Elaphoglossum, six clades were supported: (1) one grow primarily in wet montane forests and evergreen informally named ‘‘Subulate scales,’’ including all the cloud forests, either terrestrially or as epiphytes. The species with subulate scales (enrolled at the base); (2) genus is distributed worldwide in the tropics with some the Lepidoglossa clade, sister group of the ‘‘Subulate species represented in temperate regions to 39° of north scales’’ clade, characterized by phyllopodia and conspic- latitude (Azores Archipelago) and to 50° south latitude uously scaly laminae; (3) the Squamipedia clade group- (Marion Islands and South Sandwich Islands). About ing species with a long-creeping rhizome, distichously 75% of the described species occur in the American tro- arranged fronds, 1–2 mm long peg-like aerophores, pics. Nearly all the species are characterized by a trans- small fronds (less than 15 cm long), and echinulate versely elongated ventral meristele in the rhizome, spores; (4) the Amygdalifolia clade consisting of the sin- simple fronds, free veins, dimorphic sterile and fertile gle species E. amygdalifolium (Mett. ex Kuhn) H. Christ, fronds, and acrostichoid sori. The main characters used characterized by long-creeping rhizomes, hydathodes, to distinguish species are the rhizome and frond scales. phyllopodia, and reddish young fronds; (5) Platyglossa; Distinctive and morphologically uniform, Elapho- and (6) Pachyglossa. The latter clades are sister groups glossum appears to have no clear relatives among other and contain species with phyllopodia and inconspicu- ferns. Pichi-Sermolli (1968) excluded it from Lomariop- ously scaly or glabrous laminae. sidaceae and created the new monogeneric family Elaph- Based on morphology, Moran and Smith (2001) pro- oglossaceae. In contrast, other authors considered the posed 11 species pairs between Elaphoglossum species genus related to Bolbitis, Lomariopsis, Thysanosoria, from the Neotropics and Indian Ocean area (i.e., Mad- Teratophyllum, and Lomagramma in the Lomariopsida- agascar, the Comoros, Mascarenes, Seychelles, and ceae, but with uncertain affinities (Holttum, 1947; Kaur, Africa). The species pair concept designates two species 1974; Kramer and Green, 1990). The present study, that appear more similar to each other on the basis of however, focuses on evolutionary relationships within morphology than to any other species in their genus Elaphoglossum instead of its generic relationships. (Moran and Smith, 2001). This should not be confused Because of the acrostichoid sori, many species of with ‘‘sister species,’’ two species with a common ances- Elaphoglossum were originally described in Acrostichum. tor shared by no other descendant. The 11 proposed Fe´e (1845) first proposed an infrageneric classification pairs suggest that species from Africa-Madagascar do based on morphological characters such as frond shape not form a monophyletic group. and texture, and scale variations. He subdivided the Since 1993, chloroplast-coding rbcL sequences have genus into two primary groups: Oligolepideae and Polyl- been commonly used to resolve evolutionary relation- epideae. Later, Fe´e (1850–1852) recognized two addi- ships in pteridophytes at the family or higher levels tional groups: Pilosellae and Chromatolepideae. In his (Hasebe et al., 1993, 1994, 1995; Kato and Setoguchi, Monographie des Genus Elaphoglossum, Christ (1899) 1999; Korall and Kenrick, 2002; Murakami et al., subdivided the genus into two primary groups: ‘‘Ordo’’ 1999; Pryer et al., 2001; Sano et al., 2000; Wolf et al., Stenoneura, based on secondary veins without thickened 1999). Some authors examined the usefulness of rbcL vein ends, and ‘‘Ordo’’ Condyloneura, based on second- at the genus level (Dubuisson, 1997; Hennequin et al., ary veins ending near the margin and thickened at the 2003; Murakami, 1995; Schulze et al., 2001) and the best tip (i.e., non-hydathodous and hydathodous species, resolution were found among the heterosporous ferns respectively). Although ChristÕs treatment is the most (Pryer, 1999), the cheilanthoid ferns (Gastony and detailed for the genus, Mickel and Atehortu´a (1980) Rollo, 1995), Trichomanes (Hymenophyllaceae; Dubuis- found some morphological inconsistencies in his classifi- son, 1997; Dubuisson et al., 2003; Pryer et al., 2001), and cation, the most important being the separation of spe- Polystichum (Dryopteridaceae; Little and Barrington, cies with subulate scales into several unrelated groups. 2003). Nevertheless, within Elaphoglossum, despite a Mickel and Atehortu´a (1980) provided a useful subgen- good support for the monophyly of the genus, rbcL se- eric treatment of the genus with a key for nine sections quence data provided little resolution (Skog et al., 2004). and 21 subsections, taking into account morphological In the present study, two different DNA sequence re- characters from the rhizome, frond shape, frond vena- gions are used: the trnL-trnF and rps4-trnS chloroplast tion, scales, and spores. intergenic spacers. The trnL-trnF spacer is the non-cod- Given the morphological uniformity of the genus, ing, intergenic spacer between trnL (UAA)30 and trnF molecular data were expected to be helpful in depicting (GAA) exons. Because of its fast evolution, this marker phylogenetic relationships. This expectation was born is often useful for studies of closely related species (Tab- out by the first phylogenetic study of the genus, a study erlet et al., 1991).
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