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Dryopteris (Dryopteridaceae) As a Case Study

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Dryopteris (Dryopteridaceae) As a Case Study Systematic Botany (2015), 40(2): pp. 387–399 © Copyright 2015 by the American Society of Plant Taxonomists DOI 10.1600/036364415X688844 Date of publication August 10, 2015 What We Do (and Don’t) Know About Ferns: Dryopteris (Dryopteridaceae) as a Case Study Emily B. Sessa,1,2,6 Li-Bing Zhang,3,4 Henry Va¨re,5 and Aino Jusle´n5 1Department of Biology, University of Florida, Gainesville, Florida 32611, U. S. A. 2Genetics Institute, University of Florida, Gainesville, Florida 32611, U. S. A. 3Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, Sichuan 610041, People’s Republic of China 4Missouri Botanical Garden, St. Louis, Missouri 63166, U. S. A. 5Finnish Museum of Natural History, University of Helsinki, 00014, Finland 6Author for correspondence ([email protected]) Communicating Editor: Chrissen E. C. Gemmill Abstract—Ferns are the second largest group of vascular land plants after the angiosperms, but remain chronically underrepresented in studies of plant phylogeny, biogeography, physiology, and genomics. The genus Dryopteris, the woodferns, is a large group with a worldwide distribution, and recent research has made it one of the better understood fern genera and a potential model for understanding many aspects of fern biology and evolution. Here we review historical and current understanding of the genus, and outline promising avenues of future research in ferns for which Dryopteris is an ideal study system, particularly for research on polyploid complexes, biogeographic distributions, and physiological ecology. Keywords—Biogeography, hybridization, morphology, phylogeny, physiology, polyploidy, taxonomy. Dryopteris Adans., commonly known as the wood, shield, this, we still know relatively little about the effects of poly- or buckler ferns (Fig. 1), is a large leptosporangiate fern genus ploidy on fern genome organization, despite rapid advances consisting of ca. 300–350 (Fraser-Jenkins 1986; Lu 1993; in our understanding of these processes in seed plants and Zhang et al. 2012) or even 400 (Zhang et al. 2013) species. angiosperms (e.g. Jiao et al. 2011). The genus is the third largest in the family Dryopteridaceae, In this review, we summarize past and present under- itself the largest family of ferns (Smith et al. 2006; Zhang standing of the genus Dryopteris, and use Dryopteris as an et al. 2013). Dryopteris species can be found worldwide example to suggest a number of avenues for future research in temperate and montane tropical regions, with a primary in ferns where basic understanding is still lacking. We begin center of diversity in eastern Asia, and secondary centers with an overview of early studies on the genus, and then in eastern North America, Mexico, South Africa, and west- present our current understanding of phylogeny, evolu- ern Europe. Historically, North American members of the tionary and biogeographic history, and hybridization and genus have received much attention due to the hypothesized polyploidy for groups in major geographic regions of the origins of several taxa via allopolyploid hybrid speciation, world. Finally, we extend what we know about Dryopteris long thought to be a classic example of reticulate evolution. to explore what we still don’t know about ferns generally, In recent years the efforts of a number of researchers have and suggest research directions that will be essential, both in made Dryopteris one of the better-understood fern genera Dryopteris and other genera, for understanding the unique (e.g. Geiger and Ranker 2005; Li and Lu 2006a; Ekrt et al. biology and evolution of this lineage of plants. 2010; Jusle´n et al. 2011; Sessa et al. 2012a, b, c; Zhang 2012; Zhang and Zhang 2012; Zhang et al. 2012; Roux 2012; Lee The Genus DRYOPTERIS and Park 2013; Sessa and Givnish 2014; Testo et al. 2015), and have positioned it as a potential model for under- Early Work on Dryopteris and Dryopteridaceae—The name standing biogeographic patterns and the dynamics of poly- Dryopteris was given by French naturalist Michel Adanson ploid complexes in ferns. Ferns, with ca. 9,000 species in his Familles naturelles des plantes (Adanson 1763), but (Schuettpelz and Pryer 2009), are the second largest group extensive movement of taxa by researchers into and out of of vascular land plants after the angiosperms, but have his- the genus over the years has led to a contemporary Dryopteris torically received far less attention than the flowering quite different from Adanson’s. As with numerous other plants. As sister to the seed plants, ferns occupy an impor- fern genera, many of the species now included in modern tant evolutionary position (Sessa et al. 2014), and they are Dryopteris were historically placed in an enormous family characterized by unique aspects of their biology and natu- Polypodiaceae (Pichi-Sermolli 1973; Fraser-Jenkins 1986). ral history, including large genome sizes (Leitch et al. 2005; A number of these taxa were moved to the large family Bainard et al. 2011; Garcia et al. 2013) and high chromosome “Aspidiaceae” (nom. illeg.) by the late 1800s and early 1900s, numbers (Manton 1950; Britton 1953, 1974; Nakazato et al. and modern families and genera subsequently began to take 2008), separate gametophytic and sporophytic stages of the shape. Carl Christensen, who worked extensively on tropical life cycle, and relatively low levels of physiological perfor- American Dryopteris, was the first to separate the thelypteroid mance (i.e. low maximum photosynthetic rates and hydrau- and dryopteroid taxa of “Aspidiaceae” (Christensen 1906, lic conductances) compared to angiosperms (Brodribb and 1913, 1920). Ching continued work on the thelypteroids and Holbrook 2004; Brodribb et al. 2007; Watkins et al. 2010). later proposed the family Thelypteridaceae (Ching 1936, Ferns have long been thought to be particularly prone to 1940, 1963), while Holttum separated the dryopteroids into hybridization and polyploidy (Grant 1981), and Wood et al. Dennstaedtiaceae subfamily Dryopteridoideae (Holttum 1947, (2009) recently calculated that 31% of speciation events in 1949, 1959). Eventually, the former family “Aspidiaceae” was ferns are accompanied by a change in ploidy level. Despite separated into the modern families Athyriaceae, Dryopteridaceae, 387 388 SYSTEMATIC BOTANY [Volume 40 Fig. 1. Photographs of representative Dryopteris taxa. A. Immature sori of D. carthusiana.B.D. cristata.C.D. cycadina.D.D. diffracta.E.D. fragrans. F. D. intermedia.G.D. marginalis. H. Mature sori and sporangia of D. marginalis. I. D. paleolata. J. Stipe scales of D. paleolata.K.D. patula.L.D. wallichiana. A–C, E–H, K–L by E. B. Sessa; D, I–J by L.-B. Zhang. Hypodematiaceae, Lomariopsidaceae, Onocleaceae, and sensu Smith et al. (2006) into a single family Polypodiaceae, Woodsiaceae, as well as Elaphoglossaceae and Peranemataceae reminiscent of the previous system that was abandoned (Ching 1940, 1965, 1975; Alston 1956; Pichi-Sermolli 1968, 1970a; roughly 100 yr ago (Pichi-Sermolli 1973). We agree with other Fraser-Jenkins 1986). Elaphoglossaceae and Peranemataceae recent authors (Sundue et al. 2014) that this decision runs were later combined with Dryopteridaceae and the latter contrary to major advances in fern classification of the last given nomenclatural preference (Pichi-Sermolli 1970b). Sub- decade, and inhibits understanding of relationships among sequent phylogenetic analyses (Li and Lu 2006a, b; Liu et al. ferns rather than clarifying them. We advocate use of the 2007) have identified four major lineages in Dryopteridaceae, established and widely accepted classification for ferns found which is now recognized as containing ca. 25 genera (Zhang in Smith et al. (2006, 2008). et al. 2013). Recently, Christenhusz and Chase (2014) proposed Dryopteris itself has transformed considerably since the a revision to fern classification in which Dryopteridaceae was early 1900s, with numerous taxa transferred to other genera combined with five other families comprising eupolypods I while a smaller number have moved in. Its largest reckoning 2015] SESSA ET AL.: WHAT WE DO (AND DON’T) KNOW ABOUT FERNS 389 seems to have been Christensen’s reference to “nearly 1,000” also identified 13 well-supported clades within Dryopteris species of Dryopteris treated in his Index filicum (1906); around s. lat. that are supported by morphological synapomor- 300–400 species are now recognized in modern Dryopteris phies and may serve as the basis for a future taxonomic (Fraser-Jenkins 1986; Lu 1993; Zhang et al. 2012, 2013). Genera revision of the genus. To date, less than half of the taxa segregated from Dryopteris or which received taxa from it potentially belonging to Dryopteris have been included in over the course of the 20th century include Ctenitis (C. Chr.) phylogenetic analyses, and so such a revision awaits more C. hr., Lastrea Bory, Lithostegia C. Presl, Nephrodium Michx., comprehensive sampling. Stenolepia Alderw., Stigmatopteris C. Chr., and Tectaria Cav. (Fraser-Jenkins 1986). Within Dryopteris, subgeneric and sec- DRYOPTERIS IN THE AMERICAS tional classification has been addressed by several authors, notably Itoˆ (1935, 1936) who treated the Japanese and Taxonomy and Phylogeny—The American Dryopteris taxa Taiwanese taxa, Ching (1938) who treated the Himalayan have received much attention since the early 20th cen- taxa including some Chinese, Indian, and Sri Lankan spe- tury from amateur and professional botanists alike. In his cies, and Lu (1990a, b, 1999), Wu and Lu (2000), and Wu monograph on the tropical American Dryopteris taxa, Carl et al. (2013), who further revised the Chinese taxa. Fraser- Christensen included 347 species and referred to another Jenkins (1986) carried out the first and most intensive 17 in North America (Christensen 1913; 1920). The vast taxonomic study on Dryopteris worldwide. He divided the majority of these are now placed in other genera, and 225 species he recognized into four subgenera: D.subg. we currently recognize 16 species in Central and South Dryopteris, D. subg. Erythrovariae (H. Itoˆ)Fraser-Jenk., America and 13 in North America (Montgomery and D. subg. Nephrocystis (H. Itoˆ)Fraser-Jenk.,andD. subg. Wagner 1993; Mickel and Smith 2004; Sessa et al.
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