Department of Environmental and Plant Biology, Ohio University, Athens, Ohio 45701, USA. Ferns and gymnosperms are two of the most important traditionally ...
J. Plant Res. 107 : 411-416, 1994
Journal of Plant Research (~ by The Botanical Society of Japan 1994
JPR S y m p o s i u m
Phylogenetic Relationships among Ferns and Gymnosperms; an Overview G a r W. R o t h w e l l Department of Environmental and Plant Biology, Ohio University, Athens, Ohio 45701, USA
Ferns and gymnosperms are two of the most important traditionally recognized groups of vascular plants, but both are unnatural when viewed in terms of phylogenetic systematics. That is to say that neither consists of a monophyleUc group. Nevertheless, both continue to be recognized as informal groupings of plants because representatives of each have similar grades of structural and reproductive features, and because many aspects of their natural relationships remain equivocal. Monophylesis for some traditionally recognized groups of pteridophytes and gymnosperms is fairly well established, but is unresolved or highly suspect for others. The latter include ferns sensu lato, filicalean ferns, seed ferns and coniferophytes. Some recent studies also question whether conifers represent an unnatural assemblage. However, a taxon that includes the Marsileales and Salviniales recently has been interpreted to be monophyletic. Comparisons of results from phylogenetic analyses using either morphological or molecular characters provide a basis for assessing the strengths of systematic hypotheses and suggest fruitful avenues for future study. It is clear from all approaches that the greatest impediment to resolution of phylogenetic relationships is the inadequate rate at which new data are being developed. Key words : Ferns - - Gymnosperms PhylogeneUc systematics - - Pteridophytes - - Seed plants
The application of phylogenetic methodology to systematic studies of land plants has revealed that many traditionally recognized groups are unnatural because they are either paraphyletic or polyphyletic assemblages (Crane 1990). That is, such groups do not consist of a common ancestor that belongs to the group, plus all of its descendants. For example, pteridophytes consist of several distinct clades of vascular plants, some of which are more closely related to seed plants than to each other, but they do not include all of the descendants of a common ancestor. Likewise, gymnosperms are only part of the seed plant clade (Crane 1985), and must be defined by exclusion of flowering plants rather than by shared derived characters. Nevertheless, for reasons of tradition or of utility, both assemblages continue to be used as systematic groupings by many botanists.
The present contribution reviews our current understanding of land plant phylogeny with particular reference to ferns and seed plants, and explores some areas where ongoing research is addressing poorly resolved relationships. It is hoped that clarification of our concepts for the natural groups included among pteridophytes and gymnosperms will provide increased impetus to move toward more natural classifications that include only monophyletic groups (Bremer et al. 1987, Donoghue 1994). Relationships among Land Plants During the past ten years cladistic studies have dramatically increased our understanding of relationships among embryophytes, and have significantly altered popular conceptions of many groups (e.g., Michler and Churchill 1984, Crane 1985, Doyle and Donoghue 1986, Hill and Camus 1986, Bateman and DiMichele 1992). Current understanding is reflected by the general agreement between two recent summary hypotheses of embryophyte relationships (Crane 1990, Michler et al. 1994). In both of these, the charophytes (represented by Coleochaete in Fig. l) are the sister group to embryophytes, and bryophytes are a paraphyletic assemblage with mosses placed as the sister group to vascular plants (Fig. 1). Lycophytes, sphenopsids, seed plants and angiosperms form monophyletic groups, but rhyniophytes, zosterophylls, trimerophytes, progymnosperms and gymnosperms do not. Whether ferns are monophyletic or merely a grade group has not been determined by previous studies. The purpose of the present study is to emphasize that (1) neither pteridophytes nor gymnosperms represent natural groups (Fig. 1), and (2) there are several natural groups among both the pteridophyte and gymnospermous assemblages. Some of these are commonly known, but others either are not currently recognized and named, or else require confirmation of monophylesis by additional work. Ferns
Of all major tracheophyte groups, systematic relationships among ferns are the least understood (Gifford and Foster 1989, Thomas 1991, Stewart and Rothwell 1993, Taylor and Taylor 1993). There is general agreement that ferns have arisen from within the trimerophyte complex (itself a paraphyletic assemblage ; Fig. 1), but there is little
G.W. Rothwell
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EMBRYOPHYTES Vascular Plants Pteridophytes
Seed Plants Q.
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I Fig. 1. Embryophyte tree summarizing current understanding of relationships among land plants. Simplified from Crane (1990).
agreement about whether ferns are monophyletic, or whether some or all of the Cladoxylales, Zygopteridales or Stauropteridales arose from the complex separately from fern groups with living representatives. Even when only groups with living species are considered, there is disagreement about relationships among the Ophioglossales, Marattiales, Filicales, and the heterosporous, leptosporangiate genera (i.e., Hydropterids). Indeed, some workers have questioned whether members of the Ophioglossales are ferns at all (e.g., Kato 1988). Preliminary results of an ongoing numerical cladistic analyses of living and fossil ferns (Fig. 2) may be regarded as a first approximation hypothesis for fern systematics. Although the results summarized in Fig. 2 are derived from an analysis that included only 26 taxa and 33 characters, all groups of living and extinct ferns that have well-reconstructed members are represented. Psilophyton crenulatum and Pertica were included as representatives of the trimerophyte complex. Also included were place holders for sphenophytes and lignophytes. The results yielded three most parsimonious trees of 143 steps where relationships of the ferns were fully resolved. As summarized in Fig. 2, the complete consensus tree placed a clade consisting of ferns, sphenophytes and lignophytes at a trichotomy with Psilophyton
crenulatum and Pertica. In these results ferns are monophyletic and they form the sister group to equisetophytes plus lignophytes (lignophytes=progymnosperms plus seed plants ; Crane 1985). Zygopterids (plus Cladoxylon and Rhacophyton) plus stauropterids form the sister group to a clade consisting of all fern groups with living representatives. Among the latter the marattialeans plus ophioglossaleans (i.e., eusporangiate ferns) form the sister group to filicaleans and heterosporous genera (often labeled leptosporangiate ferns, Fig. 2). In agreement with recent paleobotanical and molecular studies, the heterosporous species are monophyletic (Rothwell and Stockey 1994, Hasebe et al. 1994, Raubeson et al. 1994). Filicaleans plus hydropterids are also monophyletic, but filicaleans form a paraphyletic assemblage. Because of the preliminary nature of this study the results must be viewed with caution, but some areas of the tree appear to represent much stronger hypotheses of relationships than do others. For example, monophylesis of hydropterids (Rothwell and Stockey 1994), and of hydropterids plus filicaleans (a currently unnamed clade labeled "Leptosporangiate" in Fig. 2) appears to be well supported (e.g., Hasebe et al. 1994). Likewise, a clade consisting of ferns, sphenophytes and lignophytes (also currently unnamed; Fig. 2) is consistent with the results
Phylogenetic Relationships
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FERNS
Eusporang. "Leptosporangiate"
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