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Chloroplast DNA Evolution and Systematics Ofphanerophlebia Proc. Nati. Acad. Sci. USA Vol. 85, pp. 2589-2593, April 1988 Botany Chloroplast DNA evolution and systematics of Phanerophlebia (Dryopteridaceae) and related fern genera (restriction site variation/plant taxonomy/Polystichum/Cyrtomium) GEORGE YATSKIEVYCH*t, DIANA B. STEINt, AND GERALD J. GASTONY* *Department of Biology, Indiana University, Bloomington, IN 47405; and tDepartment of Biological Sciences, Mount Holyoke College, South Hadley, MA 01075 Communicated by Warren H. Wagner, Jr., December 21, 1987 ABSTRACT Restriction site variation in chloroplast DNA neotropical in distribution. Cyrtomium, in contrast, is pri- was examined in the neotropical fern genus Phanerophiebia marily Asiatic in distribution and contains ca. 15 taxa. and in selected species of the related Asiatic genus Cyrtomium Species relationships within each genus remain poorly un- and the cosmopolitan progenitor of these two, Polystichum. A derstood, and evolutionary affinities between the two groups total of 103 restriction site mutations was identified; these were are currently controversial (16). Two competing hypotheses used to construct phylogenetic networks and trees based on have been presented to explain the presence of Old and New Wagner and Dollo parsimony and Fitch-Margoliash distance World taxa of strikingly similar structures: (i) Phanerophle- algorithms. The analyses provided evidence that Phanerophie- bia and Cyrtomium evolved independently from different bia did not arise from Cyrtomium. Both genera are convergent ancestral stocks within Polystichum on different continents descendants from different progenitor groups in Polystichum, and developed similar structural features convergently (17). and Asiatic Cyrtomium is more closely related to temperate (ii) The two groups share direct ancestry; Cyrtomium species New World Polystichum than it is to neotropical Phanerophk- evolved from an Asiatic ancestor, and the American taxa bia. Reticulate venation, previously considered an important (submerged in Cyrtomium) represent a transoceanic disjunc- taxonomic character for infrageneric classification in Phaner- tional event (18). Structurally, the two segregates differ ophiebia, most likely evolved independently twice within the primarily in details of frond dissection and venation, the genus. Diploid maternal progenitors are suggested for two of evolutionary importance of which is difficult to assess, and four tetraploid species analyzed, and species-level distinctions the overall phenotypic similarity of the species obscures for two closely related taxa of Phanerophlebia are questioned. relationships between them. We undertook a study of chloroplast DNA variation as The chloroplast genome has been shown to possess great part of general systematic studies centering on the species of potential as a tool for the assessment of evolutionary rela- Phanerophlebia, in the hope that analysis of restriction site tionships among plants. Physical and gene mapping and/or mutations would clarify some poorly understood aspects of comparative analysis of restriction endonuclease site muta- the following topics: (i) What are the interrelationships tions have been used by many workers to study problems at among the taxa of Phanerophlebia? Information from this both specific and generic levels in various plant groups independent and highly conserved data source should help to (1-10). The latter approach is particularly well suited for assess the relative importance of the structural differences studies of evolutionary divergence within species com- currently used in species circumscriptions, provide a mea- plexes, and the highly conserved nature of chloroplast DNA sure of primary divergence among the diploid taxa, and and relatively low levels of homoplasy facilitate the con- suggest a potential maternal ancestor for each of the tetra- struction of relatively unambiguous phylogenies using cla- ploids (inheritance of the chloroplast genome has been distic analysis. determined to be uniparental in Polystichum; D.B.S. and D. To date, relatively few studies have been published on the Barrington, unpublished data). (ii) Are Cyrtomium and Phan- chloroplast DNA of pteridophytes. Most of these have erophlebia monophyletic; i.e., do the Asian and American aimed primarily at characterization of the genome and species groups share direct common ancestry (with subse- general structural comparisons of fern chloroplast DNA to quent transoceanic disjunction) from a single Polystichum that of gymnosperms or angiosperms (11-14). Exceptions ancestor, or are they convergent derivatives from different are ongoing research on evolution of the chloroplast ge- Old and New World ancestral stocks within Polystichum? nomes of Osmunda species (14, 15) and a recent study on (iii) What are the levels of point-mutational (site change) divergence between chloroplast DNAs of two Polystichum variation within the large and complex fern genus Polysti- species (D. and P. Soltis, personal communication). In this chum? A detailed investigation of this topic was not the paper we present a phylogenetic analysis of restriction site intent of this work, but comparisons among a small sample mutations among chloroplast DNAs of species in the genus of species showing different distributional patterns should Phanerophlebia and of selected taxa in the closely related provide preliminary information for further research on this fern genera Cyrtomium and Polystichum. subject. Polystichum Roth (Dryopteridaceae; Dryopterideae) com- prises a large and variable alliance of about 160 species and is nearly cosmopolitan in distribution (16). Most pteridolo- MATERIALS AND METHODS gists currently recognize several segregate genera, of which The 17 samples studied are listed in Table 1 and include all the structurally similar Phanerophlebia Presl and Cyrto- extant species ofPhanerophlebia. Two additional taxa found mium Presl contain the most species. Phanerophlebia, the in some of the recent literature (19) were not studied: focus of this study, comprises ca. 9 taxa and is primarily Phanerophlebia hautensis C. Chr., a Haitian endemic not recollected since the early 1900s, is now presumed to be The publication costs of this article were defrayed in part by page charge payment. This article must therefore be hereby marked "advertisement" tPresent address: Missouri Botanical Garden, P.O. Box 299, St. in accordance with 18 U.S.C. §1734 solely to indicate this fact. Louis, MO 63166. Downloaded by guest on September 28, 2021 2589 2590 Botany: Yatskievych et al. Proc. Natl. Acad. Sci. USA 85 (1988) Table 1. Samples used in this study Sample no. Species name Source of sample Phanerophlebia 1 *Ph. auriculata Underw. United States: Arizona (Yatskievych 83-161) 2 Ph. juglandifolia (Willd.) J. Smith Mexico: Chiapas (Yatskievych et al. 85-182) 3 *Ph. juglandifolia (Willd.) J. Smith Costa Rica: San Jose (Yatskievych and McCrary 86-13) 4 Ph. macrosora (Baker) Underw. Mexico: Oaxaca (Yatskievych and Gastony 86-329) 5 Ph. nobilis (Schlecht. & Cham.) Presl Mexico: Mexico (Yatskievych et al. 85-211) 6 *Ph. pumila (Mart. & Gal.) Fee Mexico: Oaxaca (Yatskievych et al. 85-209) 7 Ph. remotispora Fourn. Mexico: Veracruz (Yatskievych and Wollenweber 83-158) 8 Ph. umbonata Underw. Mexico: Nuevo Le6n (Yatskievych and Wollenweber 83-87) Cyrtomium 9 C. caryotideum (Hook. & Grev.) Presl United States: Hawaii, Oahu (Terry et al. in 1984) 10 C. falcatum (L. f.) Presl United States: South Carolina (Yatskievych and McCrary 83-184) 11 C. fortunei J. Smith Japan: Honshu, Shiga (Mitsuta in 1984) 12 C. macrophyllum (Makino) Tagawa Japan: Honshu, Shiga (Mitsuta in 1984) Polystichum 13 Po. acrostichoides (Michx.) Schott United States: Massachusetts (Sprague in 1986) 14 Po. imbricans (D. C. Eaton) D. H. Wagner United States: California (Yatskievych and McCrary 84-119) ssp. curtum (Ewan) D. H. Wagner 15 Po. lonchitis (L.) Roth United States: Arizona (Yatskievych and Windham 85-302) 16 Po. munitum (Kaulf.) Presl United States: California (Yatskievych and McCrary 84-131) 17 *Po. scopulinum (D. C. Eaton) Maxon United States: Arizona (Yatskievych and Windham 85-297) Asterisks indicate tetraploid Phanerophlebia and Polystichum taxa. Pressed vouchers of all samples are accessioned at the Deam Herbarium of Indiana University (IND) and include more precise locality data. extinct, whereas Phanerophlebia lindenii Fourn. of southern icut, Storrs). Because the large single-copy region of the Mexico has recently been designated a minor structural Lactuca chloroplast genome contains a 22-kilobase (kb) variant of the more common Ph. pumila (G.Y., unpublished inversion in comparison with the primitive genome organi- data). We also examined selected species of Cyrtomium and zation found in most other land plants (3), the three probes Polystichum for comparative purposes. Systematic relation- containing this portion of the genome were replaced with ships in these two genera are poorly understood, and taxa in three comparable fragments of Petunia (provided by J. these groups were chosen primarily on availability of suffi- Palmer, University of Michigan, Ann Arbor), to preserve cient plant material. The five Polystichum species chosen colinearity in our analyses. Labeling of probes with 32P by exhibit three distributional patterns: eastern United States nick-translation and filter hybridizations was done as de- (Po. acrostichoides), western United States (Po. imbricans, scribed (20, 23). Groups of 1-3 adjacent fragments (9.0-18.8 Po. munitum, Po. scopulinum), and circumboreal
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