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Spore Morphology in Relation to Phylogeny in the Fern Genus Elaphoglossum (Dryopteridaceae)

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Spore Morphology in Relation to Phylogeny in the Fern Genus Elaphoglossum (Dryopteridaceae) Int. J. Plant Sci. 168(6):905–929. 2007. Ó 2007 by The University of Chicago. All rights reserved. 1058-5893/2007/16806-0010$15.00 SPORE MORPHOLOGY IN RELATION TO PHYLOGENY IN THE FERN GENUS ELAPHOGLOSSUM (DRYOPTERIDACEAE) Robbin C. Moran,1 Judith Garrison Hanks,2 and Germinal Rouhan3 New York Botanical Garden, Bronx, New York 10458-5126, U.S.A.; Marymount Manhattan College, 221 East Seventy-First Street, New York, New York 10021, U.S.A.; and Institut de Recherche pour le De´veloppement US084, Muse´um National d’Histoire Naturelle, De´partement Syste´matique et Evolution, Herbier National, 16 rue Buffon, 75005 Paris, France The perispore structure of Elaphoglossum was studied using a scanning electron microscope. Of the species examined, 119 corresponded to those used in a previously published phylogenetic analysis of the genus based on two chloroplast noncoding DNA regions, trnL-trnF and rps4-trnS. The spores of 102 additional species were examined for comparative purposes. Five perispore characters were scored for each species and optimized onto the previously published molecular tree. The morphology of the perispore and its character state changes are described and discussed in a phylogenetic context. Synapomorphies for major clades within the genus were identified, such as spines for the Neotropical species of sect. Squamipedia and perforations, spines, and cristae for subsect. Pachyglossa and a large subclade within sect. Setosa. This study is the largest done on perispore morphology in relation to phylogeny in a genus of ferns. Spore images of all species studied are available at http://www.plantsystematics.org. Keywords: Elaphoglossum, ferns, perispore, phylogeny, pteridophytes, spores. Introduction phyllopodia, and aerophores. With regard to spores, they showed that considerable diversity exists, and in some cases this diver- Elaphoglossum contains ca. 600 species and ranks as one sity corresponded to their proposed subsections or unnamed of the world’s largest fern genera. It is pantropical but most species groups. Mickel (1980, 1985) published spore images species-rich in the Neotropics, where ca. 80% of the species oc- for 24 species of Elaphoglossum, and the spores of 50 species cur. Nearly 75% of the species are epiphytes. The genus is re- of Elaphoglossum were examined by Tryon and Lugardon lated to Bolbitis, Teratophyllum,andLomagramma,asevinced (1991). These workers found the spores to be monolete and by chloroplast DNA sequence data (E. Schuettpelz, personal bilateral, to have a longitudinal laesura, and (depending on communication) and morphological characters such as acrosti- the species) to be from 20 to 80 mm long. None of the above choid sori, sterile-fertile leaf dimorphy, an elongated (in cross studies, however, assessed perispore morphology in a cladis- section) ventral vascular bundle in the rhizome, and this ventral tic framework because phylogenetic trees were lacking. vascular bundle bearing all the roots (thus, the roots appear to Rouhan et al. (2004) and Skog et al. (2004) presented phylo- be borne only on the ventral surface of the rhizome; Holttum genetic hypotheses for Elaphoglossum based on DNA sequences 1978; Kramer 1990). These genera are currently placed in the from the chloroplast genome (trnL-trnF and rps4-trnS by Rouhan Dryopteridaceae, a placement well supported by molecular phy- et al. [2004]; rbcL, trnL-F,andrps4-trnS by Skog et al. [2004]). logenetic studies (Smith et al. 2006). Unfortunately, Elaphoglos- The Rouhan et al. (2004) study was the most comprehensive, sum lacks a fossil record. containing 123 taxa from both the New and Old Worlds (as Fe´e (1845) and Christ (1899) proposed subgeneric classifi- opposed to 48 species from only the New World in the Skog cations of Elaphoglossum based primarily on frond shape, et al. [2004] study). Rouhan et al. (2004) recovered 11 main texture, scale characteristics, and the presence versus absence clades within the genus (fig. 1). These clades largely corre- of hydathodes. More recently, Mickel and Atehortu´ a (1980) sponded to the sections and subsections proposed by Mickel proposed an infrageneric classification based on sporophyte and Atehortu´a (1980). The clades (starting at the bottom of fig. morphology and spore structure as determined from images 1) can be characterized as follows. Section Amygdalifolia con- taken with a scanning electron microscope (SEM). The mor- sists of a single species (E. amygdalifolium)thathaslong-creeping phological characteristics they found useful in subdividing rhizomes, phyllopodia, and hydathodes—a unique character the genus included rhizome habit, lamina scale type and dis- combination in the genus. Its reddish young leaves are also tribution, and the presence versus absence of hydathodes, unique within the genus. Elaphoglossum aemulum (endemic to Hawaii), E. glaucum (native to Central America), and sect. Elaphoglossum are characterized by phyllopodia and usually 1 Author for correspondence; e-mail [email protected]. thick, glabrous to very sparsely scaly laminae. Based on mo- 2 E-mail [email protected]. lecular evidence (Rouhan et al. 2004), sect. Elaphoglossum 3 E-mail [email protected]. consists of two main clades, subsects. Pachyglossa and Platy- Manuscript received December 2006; revised manuscript received March glossa, although no known morphological or anatomical char- 2007. acters separate these two groups. Section Squamipedia is 905 Fig. 1 Phylogeny of Elaphoglossum. Strict consensus of 1008 most parsimonious trees based on a combined analysis using plastid DNA sequence data from the trnL-trnF and rps4-trnS regions, resulting from a heuristic search using the indel coding ID. Numbers above the branches are bootstrap percentage values >50%. Single letters in dark and light gray boxes on branches refer, respectively, to synapomorphic indels in trnL- trnF and rps4-trnS alignments. Species in boldface are from the Indian Ocean area. After Rouhan et al. (2004). MORAN ET AL.—SPORES OF ELAPHOGLOSSUM 907 characterized by long-creeping rhizomes, paired peglike aero- glossa, is characterized by laminar scales with marginal teeth phores on the rhizome near the petiole base, pale brownish consisting of acicular cells (all other Elaphoglossum species flaccid rhizome scales, and a lack of phyllopodia. The subulate- have laminar scales with marginal teeth consisting of glandular scaled clade (Subulata; fig. 1) is characterized by leaves with or bulbous marginal cells or gland-tipped marginal processes). subulate scales, that is, erect hairlike scales enrolled at the base Given the broad correspondence of sporophyte morphology and often all the way to the tip. This clade is composed of two with the groups recovered from recent molecular phylogenetic subsections: subsect. Polytrichia, which lacks hydathodes, and studies, the objective of this article is to compare spore mor- subsect. Setosa, which has them. The last section, sect. Lepido- phology of Elaphoglossum with the phylogeny of the genus. Fig. 2 Spores of Elaphoglossum. A, E. amygdalifolium (Costa Rica, Grayum 2373, NY). B, E. aemulum (Hawai, Krajina & Lamoureux 611029059, NY). C, E. glaucum (Mexico, Mickel 9675, NY). D, E. latifolium (Jamaica, Underwood 3146, NY). E, E. grayumii (Costa Rica, Grayum 3017, NY). F, E. terrestre (Costa Rica, Moraga 509, NY). G, E. marquisearum (Marquesas, Word 6390, P). H, E. guatemalense (Mexico, Martinez 14987, NY). I, E. herminieri (no data). J, E. productum (Ecuador, Øllgaard & Navarrete 105872, AAU). K, E. lepervanchei (also as aff. conforme in Rouhan et al. 2004; Mauritius, Rouhan et al. 175, NY). L, E. subsessile (Madagascar, Rouhan 432, P). Scale bars ¼ 10 mm. 908 INTERNATIONAL JOURNAL OF PLANT SCIENCES Material and Methods from the same country as that of the DNA voucher. Gener- ally, one specimen per species and 20–100 spores per stub Spores were obtained from herbarium specimens of Ela- were examined. In cases where perispore variation was sus- phoglossum at AAU, F, GH, MO, NY, P, and US. For 12 spe- pected within a species, two or more specimens were examined cies (those with vouchers are underlined in app. A), spores (e.g., E. erinaceum, E. nigrescens, E. petiolatum;app.A).Be- were taken from the DNA vouchers cited in the Rouhan sides those species included in the Rouhan et al. (2004) analy- et al. (2004) study. It was not possible to do this for most of sis, 102 additional species were imaged to assess the generality the vouchers cited because they lacked fertile leaves. For of results. The species examined for this study and voucher in- these species, attempts were made to use specimens collected formation are listed in appendix A. Fig. 3 Spores of Elaphoglossum subsect. Pachyglossa. A, E. sartorii (Mexico, Munn-Estrada & Mendoza 1683, NY). B, E. croatii (Costa Rica, Rojas 1535, NY). C, E. cismense (Costa Rica, Rojas 2877, NY). D, E. vieillardii (New Caledonia, Munzinger 1276, P). E, E. malgassicum (Madagascar, Rouhan 427, P). F, E. sieberi (Mauritius, Rouhan 176, NY). G, E. macropodium (Tanzania, DeBoer & Schippe 457, K). H, E. metallicum (Peru, Saga´stegui 14459, NY). I, E. decaryanum (Madagascar, Rasolohery 873, P). J, E. hoffmannii (Costa Rica, Hennipman 6986, NY). K, E. biolleyi (Costa Rica, Davidse et al. 28794, NY). L, E. pteropus (Brazil, Steward & Ramos P19692, P). Scale bars ¼ 10 mm. MORAN ET AL.—SPORES OF ELAPHOGLOSSUM 909 The spores were transferred with dissecting needles from her- To assess perispore evolution in a phylogenetic context, barium specimens to aluminum SEM stubs and coated with five perispore characters were scored (app. B) from the SEM an asphalt adhesive. The stubs were then coated with gold- images (figs. 2–11). Their character state changes were then palladium in a sputter-coater for 2.5 min, and spores were im- optimized, using MacClade 4.0 (Maddison and Maddison aged digitally using a JEOL JSM-5410LV SEM equipped with a 2000), onto the strict consensus tree from the analysis of the JEOL Orion 5410 software interface. The accelerating voltage molecular data (Rouhan et al. 2004). was 15 kV. Spore images of all 221 species examined for this In several instances for the presentation of results, we use dif- study (app.
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