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Home , Archaeopteridales, Cladoxylopsida, Gymnogrammitis, Lycopodiopsida, Plenasium, Psilotaceae

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ISSN 1346-7565 Acta Phytotax. Geobot. 56 (2): 111-126 (2005)

Invited article

Classification, Molecular Phylogeny, Divergence Time, and

Morphological Evolution of with Notes on

and Monophyletic and Paraphyletic Groups

MASAHIRO KATO*

Department ofBiotogicat Sciences,Graduate Schoot ofScience,Universitv. of7bkyo, Hongo, 7bk)]o IJ3- O033, lapan

Pteridophytes are free-sporing vascular land that evolutionarily link and seed plants. Conventiona], group (taxon)-based hierarchic classifications ofptcridophytes using phenetic characters are briefiy reviewcd. Review is also made for recent trcc-based cladistic analyses and molecular phy- logenetic analyses with increasingly large data sets ofmultiplc genes (compared to single genes in pre- vious studies) and increasingly large numbers of spccies representing major groups of pteridophytes (compared to particular groups in previous studies), and it is cxtended to most recent analyses of esti- mating divergcnce times ofpteridephytes, These c]assifications, phylogenetics, and divergcncc time esti- mates have improved our understanding of the diversity and historical structure of pteridophytes. Heterospory is noted with referencc to its origins, endospory, fertilization, and dispersal. Finally, menophylctic and paraphyletic groups rccently proposed or re-recognized are briefly dcscribcd.

Key words: classification, divergence timc estimate. fems,heterospory, molecular phylogcny, pteri- dophytcs.

Morphological Classifications it a recent diversification, resulting in a total of about 12,OOO species, which may be primitive or Pteridophytes, like seed plants ( and advanced. The species were classified in many difl angiosperms), are vascular land plants and also are ferent classificatien systems based on morphologi- similar to nonvascular bryophytes in the free-speringcal characters. Some of major classifications put

reproduction, Evolutionarily they fo11owed bryo- fbrward in the 20th century are briefly noted here

phytes and preceded seed plants. Thus, free-sporing ('lables 1, 2). vascular plants or pteridophytes in a broad sense Engler & Prantl (1902) classified pteridophytes have a long (420 million years) evolutionary histo- into fbur classes, Filicales, Sphenophyllales, ry, and on the other hand, like angiosperms, exhib- and fycopodia]es, and subdivided the

* PTesent address: Department of , National Science Museum, Tsukuba 305-OO05, Japan e-mail address, [email protected]

This article is fonned frem the presentation as one of contributions for the International Symposium 2004, Asian Plant

Diversity and Systematics, held at Sakura, Chiba, Japan on July 29 - August 2, 2004,

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TABLE 1 . Classifications ofmajoT ptcridophytc groups proposed by sorne authors, based on cemparative morphology, Numbers indi- cate grouping in each classification and do not correspond among classifications.

Engler & Prantt C1902) Verdooun (1938)Tagawa&Iwatsuki(1972)PichiSermolli(1977)Chmg{E97S)Tryon & TT)'on (1982) Krarner & Green (1990)

1,Lycopodiales 1,Lycopodiinae 1.Lycopsida 1.Lycephytina 1,Lycephytina1.Lycoodiepsida 1.Lycopodiatae 1-1.Ligulatae 1-1-t.Se]aginellineae1-1.Selaginel]ales1-1.Se]agine]]ales 1-1.Selaginel[ales1-1.SeiaginellRlesl-1,Selaginellales1-1,Selaginellales

1-I-2.Isoetineae l-2. 1-2.Isoetales 1-2,Jsoetales 1-2. Lycopodia]cs ]-2, Isoctales 1-2,lsoetales 1-2.Eligulatae

1-2-1.LycopDdincac 1-3.Lycopodia]es1-3.Lycopodiales 1-3.Lycopodjales 2.Isocphytina 1-3.Lycopodiales1-3,Lycepodiales 1-2-2.Psilotineae 2.Psi]ophytinae 2,Psi]opsida 2,?sjophytina 3,Psjophytina 2.Psilotatae

2.Equiestales 3.Articulatae 3,Equisetopsida 3.Sphenophytina4, Sphenophytina 2.Equisetopsida 3.Equisetatae 3,SphenophylLates

4.Filica]es 4. Filicinae 4.Pteropsida 4.Filicophytina 5.Fi]icophytina3.Fiticopsida 4.Filicatae (incl.Psilotaceae) Extinct group included in Equisetopsida in other classifications,

TABi.E 2. Classifications ofmajor groups proposed by some authors, based on comparative morphology. Numbers indicate group- ing in each classification and do not correspond among classifications. Christellsen(l938)Cepeland(1947)Tagawa&iwatsuki(1972)PichiSermolli(1977)Ching{IY7S) Tryon&Tryen(1982) 1,Eusporangiatae 1.Eusporangiopsida 1,Polypodiidae

1-].Ophioglossales ] . Qphioglossales1.0phioglossales 1,Ophioglossopsida 1-1,Ophioglossales 1-1.0phioglossales 1-2,Maradiaies 2.Marattiales 2.Maraniales 2.Marattiepsida 1-2.Marattia]es 1-2.Marattiales 2,Leptosporangiatae3. FiHcales 3.Filicales 3,Fllicopsida 2,Protoleptosporangiopsida1-3.PojypodiaLes 2-1.Filicales 3-].Osmundjclae 3.Leptosporangiopsida t-3-1.Po]ypodiineae 3-2,Plagiogyriidae 3-t,Po]ypodiales 3-3.Gleicheniidae 3-4.Schizaeidae 3-5,Hymenophyllidae

2-2, Salviniales 4. Salviniales 3-6,Salvinlidae 3-2,Salviniales t-3-2.Salviniineae 5.Marsileales 3-1,MarsiTeidae 3-3,Marslleales 1-3-3.Marsiteineae 2. Psilotidae

class Filicales into three orders, Filicales leptospo- and in total 14 families including the Iarge family

rangiatae (suborders Eufilicineae and Hydro- with 15 subfamilies. Ching (1940) "Polypodiaceae" pteridineae), Maiattiales and Ophioglossales, and the classified into 33 families and rec- "Poly- class Lycopodiales into two orders Lycopodiales ognized five series in the polyphyletic eligulatae including suborder Psilotineae and podiaceae" in the context of phylogeny, Ching Lycepodiales ligulatae with suborders Selaginetli-(1978) classified Chinese pteridophytes (division neae and Isoetineae, Christensen's (1905, 1913- Pteridophyta) into five subdivisions: subdiv, 1934) Index Filicum and supplements I-III enu- Lycophytina comprising orders Lycopodiales and

merated all fern species ofthe world described, In SeJaginellales, three monotypic subdiv, Isoephytina,

his systematic classification of Christensen Sphenophytina and Psilophytina, and subdiv. (1938) recognized two series (Filices EusporangiataeFilicophytina comprising three classes (Eusporan- and Filices Leptosporangiatae), two orders giopsida [orders Ophioglossales and Marattiales], Ophioglossales and Marattiales in the former series Protoleptosporangiopsida [Osmundales], and and two orders Filicales and Salviniales in the latteg Leptosporangiopsida [ or Filicales,

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Marsileales, Salviniales]). In Genera Filicum (suborders Polypodiineae, Marsileineae, and Copeland (1 947) recognized orders Ophioglossales Salviniineae), and divided into (1 family), Marattiales (1 family), and Filicales (19 bycopodiales, Selaginellales and Isoetalcs. Ttyon & families including and ), Tryon (1982) included Psilotaceae in Filicopsida Holttum (1949) classified leptosporangiate ferns (ferns) based on BierhorsVs (1977 and references into 14 families including the large family Denn- cited therein) morphological and anatomical results

staedtiaceae with 1 1 subfamilies and proposed three and wall characters. phylegenetic lineages, ofwhich one is terrninated by In short, the classifications based on phenetic rlagawa Dennstaedtiaceae. & Iwatsuki (1972) adopt- characters usually recognized four major groups ed the conventional classification ofpteridophytes of living pteridophytes, among which ferns were

into four classes Psiopsida, Lycopsida, Equiset- divided into Marattiales, Ophioglossales and

opsida, and Pteropsida. They classjfied Pteropsida Filicales, although certain groups (e.g., Psilotaceae into erders Ophioglossales, Marattiales, Filicalcs, and aquatic ferns) were assigned to different groups Marsileales, and Salviniales. [lagawa & Iwatsuki ofhigher ranks or treated at different ranks ([lables

(1972) recognized in total 34 families for pterido- 1, 2). Characters that are infbrmative throughout phytes of Thailand. Pichi Sermolli (1977) classified pteridophytes are not many. Those classifications Pteridophyta into fbur subdivisions, Lycophytina, with hierarchic ranks are generally taxon-based and Sphenophytina, Psilophytina, and Filicophytina, have usually not been given statistically analyzed

The first three were monotypic each with single interrelationships of families.

classes, while the last Filicophytina comprised three

classes, Ophioglossopsida, Marattiopsida and Molecular Phylogenies

Filicopsida. Pichi Sermolli (1977) assigned 58 of64 families to Filicopsida, 3 to Lycopsida, 1 to Achievement ofmelecular phylogeny, which is dis- Equisetopsida, and 2 to Psilotopsida. Kramer & played as a phylegenetic tree, succeeded long con- Green (1990) compiled contributions to pterido- tributions of systematics, classifications, and fio- phyte classification and presented a similar classi- ras based on phenetic or morphological characters, fication system of four classes Psilotatae (1 family), as noted above, Molecular analyses with large data Lycopodiatae (3 families), Equisetatae (1 family), sets dealing with all or most groups and Filicatae (33 families). Among families of have been explosive since the middle 1990s. One Filicatae, affinities were suggested between year later than Chase et al.'s (1993) epoch-making Dipteridaceae and Cheiropleuriaceae; Vittariaceaestudy on angiosperm phylogeny using a large data and Pteridaceae; tree fern families; Lomariopsida- set (ca, 500 operational taxonomic units), Hasebe et ceae, Davalliaceae, Nephrolepidaceae, Oleandra- aL (1994) presented a molecular phylogeny oflep-

ceae and Dryopteridaceae; Polypodiaceae and tosporangiate ferns deduced from rbcL sequences of

Grarmnitidaceae; and Azollaceae and Salviniaceae.58 species representing almost all farnilies recog-

Tryon & Tryon (1982) divided Division nized in the then classifications (Kramer & Green

Pteridophyta into three classes Filicopsida, 1990). The number of families they dealt with was

Equisetopsida (with a single order Equisetales) and 1arger than that of any previous molecular analyses, Lycopodiopsida, and subdivided Filieopsida into although the number of species per family was few. two subclasses Po]ypodiidae and Psilotidae. Tryon Hasebe et al,'s (1994) pioneer work solved several & Tryon (1982) further divided Polypodiidae into of significant questions on pteridophyte phylogeny

orders Ctphioglossales, Marattiales, and Polypodiales and accelerated research to solve them, One of their

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kgg=uttsE @ Clade4 0 MarsileaRegnellidium n=ep-oEEege'opt PilulariaAzollaSalvinia Clade3

Clade 2Clade

1Davalliaceae

y<,sgeSes if4s,¢

8sa.oEoE 8saa 8xsgBgc8-xa-!paas6wh6m £ sin?m

FiG. 1. Monophyletic and paraphyletic groups ofpteridophytes. A. Monophyletjc aquatic ferns. Aiolta and Satvinia are assigned to Salviniaceae or each , to monotypic family. Tree is adapted from Pryer (1999). B. Monophyly of Polypediaceae and Grammitidaceae (polygrarnmoids) and that ofepiphytic polygrammoid ferns and Davalliaceae. Four clades ofpolygrammotd fenis are defined by Schneider et at, (2004b). Selid trianglc in clade 4 indicates Grammitidaceae. C. Majer greups ef polysperan- giophytes. Groups on the right side are monophyletic, and groups en the top are paraphyletic. Protracheophytes may be para- phylctic. Part ofdrawing is modified from Pryer et al. (2004b).

findings is that feims that were considered primitive or apical annulus. The of Hymeno- by morphological systematics diverge earlier than phyllaceae and Gleicheniaceae has an oblique annu- morphologically more advanced groups. For exam- lus, while higher leptosporangiate ferns have small, ple, are the basalmost in leptospo- flattened sporangia with vertical annuli. It is hypoth- rangiate ferns, and Hymenophyllaceae and a group esized that the sporangium morphology evo]ved of Gleicheniaceae, Dipteridaceae (also Cheiro- from a massive to small capsule and from the dista1 pleuriaceae) and Matoniaceae are the second and to oblique and then to vertical annulus (Bower

third basa], In comparison, Vittariaceae, Pteridaceae, l935).

Polypodiaceae, Davalliaceae, Dryopteridaceae, and The second of their findings is that tree fern

seme others are branched 1atez This order ofbranch- families, Cyatheaceae, Dicksoniaceae and Metaxy-

ing is in good accordance with the polarity of trend aceae, along with Plagiogyriaceae, are mono- of sporangia. The sporangium of Osmundaceae is phyletic, although Plagiogyriaceae are not typical-

massive and, along with Schizaeaceae, has a lateral ly tree ferns. Traditionally, the two tree fern families

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are considered not to be closely related by differ- fer in a few characters. Polypodiaceae usually have

ences in dermal appendages and sori: Cyatheaceae reticulate venation and only scales as appendages,

are characterized by having scales and superficial while Grammitidaceae have free venation and aci-

sori, and Dicksoniaceae, by having hairs and mar- cular hairs besides scales, Later, a multigene phy- ginal sori. Metaxyaceae, like Plagiogyriaceae, show logenetic analysis with much ]arger data sets shows

a combination of hair appendages and superficial that Gramrnitidaceae are nested within Polypodia-

"poly- sori (soenosori), Recently, Hymenophyllopsidaceae,ceae and the two families are together coined a small nontree fern family endemic to the grarnmoid" ferns (Schneider et al. 2002, 2004b), Venezuelan Guayana, Guyana and Brazilian sand- Furthermore, this polygrammoid group and stone highlands (tepuis), were unraveled to have a Davalliaceae differ in that the sori are marginal and close relationship with the tree fern group (Wblfetindusiate in Davalliaceae and superficial and exin- al. 1999). It supports monophyly ofthe tree fern and dusiate in the polygrammoid group. Comparison related nontree fern families. Hence, this tree-fern with their successive sisters (e,g., Oleandra,

clade saw marked evolutienary changes in stern AJI?phrolepis, and Arthrqpteris) indicates that the

habit, dermal appendage, lamina histology, soral exindusiate sorus of the polygrammoid fems is an position, and indusium. apomorphic character state. By contrast, they share The third of Hasebe et al.'s findings is wonhy densely scaly, long-creeping, dorsiventral T`hizornes of special mention. It is that the aquatic and het- (but the are short and the are radi- erosporous fern families, Azollaceae, Marsileaceae,ally arranged in many Grammitidaceae), a com-

and Salviniaceae, fbrm a mQnophyletic clade (Fig.plex dictyostelic vascular system ofthe , and 1A). Aquatic life and heterospory are usually con- epiphytism. Davalliaceae and the polygrammoids,

sidered to be a curiously enough sharing, because like Vittariaceae, are typical epjphytic fern families.

the families are so distinct in the vegetative and The monophyly suggests the origin ofthe epiphyt-

reproductive characters as to be placed distantiy or ic families from a common ancestor of a certain life

ctassified at higher ranks in traditienal classifica- form, tions, as noted above. Rothwell & Stockey (1994) Phylogenetic analyses using increasingly large discovered a fern, Ilydmpteris, and inter- data sets in the number of groups and the length of preted that it has intermediate morphologies between DNA sequences fbllowed. Hasebe et aL7s (1995)

Marsileaceae and Salviniaceae. Rothwell & Stockey analysis with more species Emd families than Hasebe

(1994) recognized the order Hydropteridales com- et al. (1994) presented simjlar results. In an analy- prising the fossil Il}pdmpteris and the extant - sis with 35 species of ferns and fern allies (i.e.,

ceae, Marsileaceae and Salviniaceae. Hasebe et , Eguisetum, and Psilotaceae) and mul-

al.'s (1994) molecular evidence is in good accor- tiple genes (three chloroplast genes and a nuclear dance with Rothwell & Stockey's (1994) treatment gene), Pryer et al. (2001) fbund noteworthy rela- of the aquatic fern farnilies. Monophyly of the tionships of lower pteridophytes. Tracheophytes

aquatic ferns is also supported by a combined mol- diverge first into the rnicrophyllous lycophytes and

ecular and morphological analysis (Pryer 1999), the euphyllous plants (Fig. 1C). This divergence is The combination of aquatic life and heterospory in fu11 agreement with the one that had been pro- will be discussed below. posed from the chloroplast gene order (Raubeson & The fburth of their findings is monephyly of Jansen 1992), The euphyllous plants diverge into

Polypodiaceae, Grammitidaceae and Davalliaceae seed plants and euphyllous pteridophytes called (Fig. IB). Polypodiaceae and Grammitidaceae difl monilophytes. The monilophytes in turn comprise

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euspQrangiate and leptosporangiate ferns, Because those differences are equally large between

Psilotaceae, and . Psilotaceae fbrm a the fbur groups, the pteridophytes were usually clade with the eusporangiate Qphioglossaceae, while classified on the class level, are

Eguisetum fbrms another clade with the eusporan- morphologically more similar te other megaphyllous

giate though support is low, fems than to Psilotaceae, although molecular evi- Pryer et al, (2004b) extended their analysis dence suggests monophyly, The most conspicuous fbr 62 taxa, using the same four genes, and con- difference between Ophioglossaceae and Psilotaceae stmcted almost the same phylogenetic tree as that of is the presence or absence of the root, but it is Pryer et aL (2001), although there is a difference in uncertain whether the root was lost in Psilotaceae or the position of Gleicheniaceae, Matoniaceae and it never appeared at the appearance ofthe family. It Dipteridaceae (including Cheiropleuriaceae). After is the case with Equisetum. The largest difference

the divergence of 0smundaceae, the rest of lep- from Marattiaceae is seen in the reproductive organ

tosporangiate ferns divides into Hymenophyllaceae and phyllotaxis. It is hypothesized that the sporan- and all others in Pryer et aL's (2001) tree, whereas in giophorous and whor]ed leaMes appeared in Pryer et al.'s (2004b) tree a monophyletic group the early divergence of Equisetopsida. Thus, the of Hymenophyllaceae along with Gleicheniaceae, molecular phylegeny suggests that remarkal)le mor- Matoniaceae and Dipteridaceae diverges from the phological diversification may have occurred in the remaining of ferns. Matoniaceae differ from the early evolution of the basal euphyllous pterido- sister-group Dipteridaceae in that the former have phytes.

discrete indusiate sori and the latter have acrosti- choid exindusiate sori (i.e. sporangia are scattered), Divergence Time although they share hairs (scales absent). The phy- logeny that the exindusiate Gleicheniaceae are like- As molecular data haye been accumulated fbr pteri- ly sister to the Matoniaceae-Dipteridaceae clade dophyte phylogeny, analyses with large data sets (Hasebe et al. 1995, Pryer et al. 2004b) supports that have been extending to estimating the divergence the extant and fossil Matoniaceae with peltate indu- times ofmajor groups ofpteridophytes, In penalized

sia were deriyed from exindusiate members of the likelyhood analyses of ferns and angiosperms,

family (Kato & Setoguchi 1999). Schneider et al. (2004a) demonstrated that most The above results show sharp conflict to the polypodioid (in a broad sense) or higher leptospo- traditional classifications of pteridophytes based rangiate ferns diversified in the (100 on comparative motphology, with special reference Mya or later; Mya = million years ago) after angio- to Iower groups. Previously, pteridophytes were sperm radiation. They further sttggested that the usually classified into ferns (Filicopsida) and three fern diversification was an ecological opportunistic classes of fern allies, i.e. Psiopsida, Lycopsida, and response to the diversification of angiosperms, as

Equisetepsida (Fig. IC). The Lycopsida is defined angiosperms came to dominate terrestrial ecosys- by the monosporangiate microphyllous leaves. tems. Recently, an unconventional photoreceptor Psiopsida is characterized by the absence of roots phytochrome 3 was discovered in a polypodioid and typical leaves, while Equisetopsida is charac- fern, Adiantum pedatum (Kawai et al, 2003). terized by the strobilus comprising sporangjophores Phytochreme 3 functions for red-light-induced pho-

with inwardly oriented sporangia and the whorled totropism and for red-light-induced chlorop]ast pho-

sphenophylls. Filicopsida has megaphyllous leaves torc]ocation, thereby conferring a distinct advantage bearing aggregates of sporangia (called sori). under low-light canopy conditions. Schneider et aL

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(2004a) argued that the photoreceptor was involved logical changes between O. cinnamomea and O. in the diversification of ferns in angiosperrn-domj- claytoniana since the earliest diyergence of the

nant dense forest ecospaces. extant Osmundaceae, as also shown by fossil evi-

A similar divergence time estimate, together dence ( O. cdytoniites). Yatabe et aL (1999) with molecular phylogeny) was undertaken for basal estimated the divergence time to be 294 or 322 fems (Pryer et al. 2004b). Using penalized likeli-Mya for the two species, 210 Mya between the hood analyses of melecular data and constraints group of 7bdea and Leptqpteris and the rest ofthe

from a reassessment of the fossil record, Pryer et aL familM and 150 Mya between the O. jmponica group (2004b) estimated that basalmost fern families and subgcnus Plenasium. diverged during the and . A Another divergence time estimate was made

most basal fern clade of Ophioglossaceae and fbr extant lycophytes based on rbcL sequences Psilotaceae appeared near the end ofthe (Wikstr6m & Kenrick 200l). By calibration using (364 Mya) and the two families diverged in the several fbssil evidence constraints Wikstr6m & Late Carboniferous, while that ofMarattiaceae and Kenrick (2001) estimated that the divergence time of Equisetaceae appeared in the very Early Caifboni- the ligulate heterosporous group (, Setagi- ferous (359 Mya) and the families diverged shortly nella) and the nonligulate homosporous fycopodia- after (354 Mya). Osmundaceae, the basalmost lep- ceae is 393 Mya, that oflsoetes and Setaginella is tosporangiate ferns, diverged in the middle 375 Mya, and that efHmperzia (also ) Carbeniferous (323 Mya), Exceptionally, Hymeno- and a group of LIFcopodium and is phyllopsidaceae, a nontree-fern member of the 351 Mya. Data suggest that, in sharp contrast, the lower tree fern group, diverged much later in the diversification of epiphytic species of Htipereia, Late [[lertiary. Two aquatic fern families, Azollaceae and likc polypodioid ferns, occurred in the

Salviniaceae, diverged in the Cretaceous. Cretaceous subsequently to the diyersification of

Among recent progress in the systematics and anglosperms, divergence time estimate ofparticular fern groups, Des Marais et al. (2003) perfbrmed a rnolecu- most noteworthy is Yatabe et al.'s (1999) work on lar analysis of Equisetum. They found that subgen-

Osmundaceae, Traditionally, bascd on morpholog- era Himpochaete and Equisetum are each mono-

ical data, Osmundaceae are classified into three phyletic, except fbr E. bagotense whose placement genera, , Leptopteris and 7bctea, among is arnbiguous. Divergence time estimation shows

whieh Osmunda are subdivided into subgenera that the modem Equisetum began divergence in the Osmundu, Osmundostrum and Plenasium (some- Early Cenozoic (Eocene; 40 Mya) and the two sub- times raised to genera), By marked contrast to this, genera diverged in the Oligocene (30 Mya), i,e., Yatabe et aVs (1999) rbcL tree shows that O. cin- much later than the origin of Equiseta- namomea is sister to all other members ofthe fam- ceae. The estimate is in accordance with fbssil eyj-

ily including O. ctaytoniana, although the two dence. A distinct gap between the two divergence

species are usually assigned to subgenus Osmuncin- times indicates that cladogenesis seldom occurred or,

strum. Osmundaceae except fbr O, cinnamomea more likely, often happened during the

diverge into two clades. One comprises 7bdea and period.

Leptopteris and the other comprises O. claytoni- In conclusion, molecular divergence time esti-

ana and a subclade comprising a subgroup of O. mates have demonstrated a historical structure of y'oponica, O. Iancea and O. regalis and subgenus pteridophytes fbr over 400 million years. Estimation Plenasium. This phylogeny suggests tittle morpho- will become more accurate, as fossil and melecular

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118 APG Nbt. 56

data will be added and calibration methods will be cheophytes (Kenrick 2000). Kato & Akiyama (in improved. press) interpreted that the branched axis of the poly- sporangiophyte with a persistent apical meristem is

Cladistic Analyses a novel vegetative organ interpolated into the

bryophytic life cycle, and the

Pryer et aL (1995) undertook the first cladistic is an archaic sporangium with the fbot, The nonva- analysis of phylegenetic relationships and mor- scular polysporangiate plants had hydroid-like con-

phological evolution of ferns, They used 77 vege- ducting cells without secondary walls, The vascular

tative and reproductive characters fbr 50 taxa rep- system increasingly developed as the axes enlarged. resenting all major groups. Pryer et al. (1995)Early vascular plants had three different types oftra- hypothesized an evolution ofsporophytic and game- cheids, S-type (e.g., Senicaulis of Rhyniopsida), tophytic characters, on based a phylogenetictree G-type (e.g., of Zesterophyllopsida), constmcted from combined morphological and mol- and P-type (e.g., PsilopItyton of Euphyllopsida) ecular data. The characters examined include vena- (Kenrick & Crane 1997). S-type tracheids have

tion, hydathodes, dermal appendages, sporangial helical wall thickenings comprising a thin decay- annulus and stalk, exospore, hairs, resistant inner layer (facing the primary cell wall) antheridium position, and the nurnber ofantheridi- and a spongy outer layer. G-type tracheids have

um wall cells. annular thickenings comprising a decay-resistant

Rothwell (1999) investigated the cladistic phy- inner layer and a nonresistant outer layez P-type tia- logeny ofpteridophytes using morpho]ogical char- cheids had scalarifbrm thickenings comprising a a ters ¢ ofboth living and fbssil plants, with special decay-resistant inner layer and pit chambers, and a reference to fems in a br.oad sense. Stauropterid nonresistant layer, with G- and P-type tra-

ferns (fossils) are a monophyletic group that is cheids are grouped in eutracheophytes, while basal in the pteridophytes and sister to the rest ofthe Rhyniopsida with simple S-type tracheids is primi- plants. Psilotaceae is next basal and most closely tive tracheophytes placed outside the eutracheo- related to extinct vascular primitive plants, phytes. Friedman & Cook (2000) stressed the hypo- Cladoxylalean ferns plus Zygopteridalean ferns thetical evolution of developmental elaboration

(both ofwhich are fossils) form a clade that is more involving thickening of the decay-resistant layer,

closely related to equisetophytes and seed plants from S-type to G-type, then to P-type and eventually than to other groups offemlike plants, [[he basal fi1- seed-plant type with no decay-prone layer. icalean ferns include living basal ferns and the Living eutracheophytes are divided into

that are considered to Paleozoicferns becoenopterid tycophytina and Euphytlophytina. This biphyletic ferns, Differences between Rothwell's (1999) and classification is in agreernent with two branching molecular phylogenies merit further analyses, patterns ofroots in pteridophytes, i.e., apical and

because the former dealt with both 1iving and extinct dichotomous branching with exogenous origin in

plants, while the latter dealt wnh ljving plants alone. lycophytes and subapical or monopodiai one with Kenrick & Crane (1997) canied out a large- endogenous origin in ferns + Equisetum (Kato & scale cladistic analysis efearly 1and plant evolution, Imaichi 1997). Zosterophyllopsida ofLycophytina basedon evidence from both fossil and extant plants. has enations on axes and Lycopsida has micro-

According to them, polysporangiate pretracheo- phyllous leayes, which are derived from enations.

phytes with multiple sporangia on branched axes Leafy Euphyllophytina has euphyllous leaves and Aglaopbyton, (e.g., Hbrneqp]tyton) preceded tra- ancestral fossils had leafless branch systems or

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A9d

Heterospory @ o

o 9)g

Homospory o 9dU o

Sporc - Dispcrsal - Fertilization

Fic]. 2. Hypothetical spore dispersal and subsequcnt fertilization in hetcrosporous ptcridophytes, compared with those ofhomesporous pteridophytes. In homesporous plants cither intragaJnetophytic sclfing or intcrgametophytic crossing occurs in bisexual game- tophytes deriyed from separately dispersed . are exosporic. In heterosporeus plants co-dispersal ofmegas- pores and microspares rnay occur by sarne migrating vector oT spore pollination, and intergametophytic crossing occurs between connected or nearby unisexual gametophytes, Garnetophytes are endosporic.

primitive leaves. Euphylls are considered to have groups during the Middle Devonian been derived from telomes, i.e., ancestral branched and (Bateman & DiMichele 1994, Bateman axes, but to have appearcd independently in differ- 1996), They are Lycopsida (Selaginellales [extant ent lineages (at least ferns, , and ] and Rhizomorphales [Isoetes]), equisetophytes), Beerling et al, (2001) and Osborne Zosterophyllopsida (Barinophytales), Sphenopsida et aZ. (2004) suggested that changes of the Devonian (some Sphenophyllales), Pteropsida (Stauro- atmospheric environment (C02 concentration, tem- pterida]es), and Progymnospermopsida (some perature) and the histological structure of leaves Aneurophyta]es, some Archaeopteridales, (stomata density, surface area, conducting system) Protopityales, Cecropsidales, and some Noeg- forced the long (40 million years) delay of evolution gerathiales), In comparison, a few heterosporous ofmegaphylls behind leafless axes or microphylls. ferns or Pteropsida (Salviniaceae [SZzlvinia, Azolla], Marsileaceae [imrsilea, Pilulania, Ragnellidium], Heterosporous Pteridophytes PlaCyzoma) evolyed more recently, probably in the Jurassic or later (Pryer et al. 2004b). Thus, het-

Heterospory is considered to be an evolutionary erospory appeared iteratively throughout the his-

prerequisite tQ a secd habit. A group of hetero- tory ofpteridophytes. Heterospory did not evolve in sporous progymnosperms evolved into seed plants, early vascular plants such as Cooksoniopsida,

which have thrived in the Mesozoic and Cenozoic, Rhyniopsida, Trimerophytopsia and

most remarkably as angiosperms in the Tertiary up that lived fi'om the Late to the Early

to the present. This clade ofprogymnosperms and Carboniferous. seed plants is coined lignophytes characterized by Heterospory is Iinked to gametophyte unisex- the secondary vascular tissue, Heterospory appeared uality: megapores exclusively produce female at minimum 10 times in most (5) ofmajor lower megagametophytes and produce rnale

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microgametophytes (Fig. 2). It results in obligate archegonia. After one or several cell diyisions the intergametophytic outcrossing, which maintains becomes a prothallial cell and (an) genetic variations that provide source ofevolution to antheridium initial(s), and subsequently it (they)

be selected. In this aspect, heterospery is mere develop(s) into antheridia, which are embedded or

advantageous than homospory that allows intraga- protmded (Smith 1955). The rnegaspore undergoes metophytic selfing, although it is more disadvanta- cell divisions in the distal part and free nuclear geous in that dispersed spores, if single, cannot divisions in the rest, and archegonia are formed in FIIius, lead to fertilization and colonization in a new loca- the cellular dista1 tissue. the male gametophyte tion except for apogamy Platyzoma shows incipientis mostly antheridial, while the female gameto- heterospory (Tryon 1964). The is two phyte has foed reserves that are alse provided to the

times larger than the microspore, a small size difi embryo. Sexual organ differentiation occurs at the

ference compared to about 1O times 1arger megas- initial stage of gametephyte development, and the pores of genuine heterosporous pteridophytes, The female garnetophyte bridges the sporogenesis and

microspore germinates and develops into a small fi1- embryogenesis. amentous (exosporic), male gametophyte, while In heterosporous plants sexual determination is the megaspore develops into a 1arge spatulate female sporophytic and, unlike that ofhomosporous plants, gametophyte, which forms lobes with antheridia, is not infiuenced by the environment. DiMichele eyentually becoming hermaphroditic (Duckett & et at, (1989) and Bateman & DiMichele (1994) Pang I 984). Subcultured portions ofthose gameto- argued that the precociousness for endospory and phytes originating from either spores yield male, gametophyte sexual maturation may possibly be a female and hermaphroditic gametephytes at various result ofa kind of heterochrony (i.e., progenesis). proportions. Results indicate that the species has an Earlier ideas of gradual evolution (e.g., Tiffhey association between gametophyte morphogenesis 1981) claim that heterospory with exosporic uni-

and sex organ formation, but the association is not sexual gametophytes, as seen in Platyzoma, is an absolute. In Ceratopteris thalictroides (Schedlbauerevolutionary intermediate between homospory (and 1976) and other homosporous fems, larger spores exospory) and heterospory with endosporic game-

from a unimodal spore-size range tend to develep tophytes. Even though endospory fbllowed het-

into bisexual gametophytes and the smaller into erosporyi endospory may have occurred unneces-

males, a similar sexual expression to that of sarily simultaneously in the megaspore and micro-

Platyzoma. Duckett & Pang (1984) compared the spore. DiMichele et al. (1989) and Bateman & sexual behavior of gametophytes ofhQmosporous DiMichele (1994) do not support this gradual evo- ferns with mixed and allopatric er allochronic lution hypothesis because of the disadvantage that gametangia, and suggested that such association of free-living (exosporic) unisexual gametophytes can- gametophyte dioecism and dimorphism evolution- not control the sex ratio and lose sexual flexibility arily may have preceded true heterospory, and sex (e,g,, lacking of intragametophytic selfing). determination may have been accelerated from the DiMichele et aL (1989) and Bateman & DiMichele gametophyte stage to sporogenesis, (1994) insist that heterospory is not a necessary Endospory is exclusively associated with het- antecedent to endospory, but rather may have erospory in living pteridophytes (Fig, 2), In evolved as an epigenetic consequence of endospory, endosporic species the gametophyte develops while They hypothesized that gametophytic unisexuality is a most portion is enclosed within the spore wall a position effect of the metabolic microenviron-

and precociously produces either antheridia or ment for developing spores: with female

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August 2005 KIY]]O: Pteridophyte phylogeny and evolution 121

gametophyte sexuality are produced at the tip ofthe andror physical connection ofmicrospores on the soral receptacle that receives much nutrient sup- megaspore surface before dispersal (Webster 1979, ply, and microsperes with male gametophyte sexu- Takamiya 1999) (Fig. 2). This microspore-on- ality are produced at the sides with less supply. megaspore connection may be called spore polli- This may be applicable for aquatic ferns (Mti"siiea,nation, compared to the po]len-on-stigma or SZitvinia, Azolla) with such a soral structure, but micropyle pollination in seed plants. Co-dispersal of

not obvious fbr Slelaginella without comparable separate microspores and megaspores andfor spore-

positional relationships. The evolution of het- pollinated megaspores by the same vector {s likely erospory and endospory (and alse endosporangy inevhable for oceanic island species that migrate by

related to the origin of the ovule) needs further long-distance dispersal. There are some endemic

analysis, heterosporous pteridophytes on oceanic islands, Heterospory is present in aquatic pteridophytese.g., lsoetes hawaiiensis, Mdms'ilea villosa, Setagi-

with an exception of SeifagineUa, which might be nella arbuscula, and S. doj7exa of the Hawaii secondary terrestrial plants retaining air cavities (Palmer 2003) and S. bonincola (?) of the Bonin around the vascular tissue, Heterosporous plants Islands (Iwatsuki et al. 1995), It is more probable

dominated tropical aquatic and amphibious habitats that colonizers of these species were established through most of the Carboniferous (DiMichele et aL by co-dispersal rather than by independent dispersal. 1985, 1992). Tliey suggest that heterospory evolved Spore pollination may happen between difftrent

in aquatic or semi-aquatic environments. Aquatic or in the same sporophyte, and off

environments are favorable for the release ofsper- spring resulting from spore selfpollination has as

matozoids and eggs, which are produced from fast- low genetic variability as that from self pollina- developing, short-lived gametophytes, and for the tion, Limited co-dispersal of selflpollinated spores consequent aquatic fertilization. These gameto- rnay promete isolation and speciatien. Spore self phytes exhibit a very shorter tirne lag from spere pollination may have a disadvantage with potential

rnaturation to fertilization in, e.g., imrisitea than inbreeding depression,

those of homosporous ferns (Schneider & Pryer This disadvantage might have been overcome 2002), Bateman & DiMichele (1994) regarded by gymnosperms with dioecism in the lineage of endosporic garnetophytes as effectively functioning lignophytes. Fossil data suggest that hydrasperman as gametes. in this context it cannot be ruled out that ovules or preovules with a salpinx (lagenostome) certain progymnosperms that evolved into seed surrounded by a dista11y divided integurnent evolved

plants had been aquatic or amphibious heterosporousinto modern ovules with a micropyle formed by a pteridophytes. Ifit is the case, the early evolution of cupulate integument (Rethwell & Scheckler 1988). seed plants might have been accompanied with The increasing eMciency ofpollen capture by the

habitat transfer from aquatic to terrestrial environ- complete integument, as shown by a wind-pollina-

ments. tion experiment using preovule and evule models Prior to fertilization, heterosporous pterido- and pseudopollen, is suggested to have been a dri- phytes have to undertake successfu1 dispersal. Both ving force for fusion ofintegumentary lobes (Niklas megaspores and microspores must be dispersed 1981). Whether (pre)ovules facilitated cross polli- within short distances to undergo intergametephyt-nation in early heterosporous gymnosperms is an

ic fertilization. This situatien may be achieved by interesting issue with reference to the evolution of

chance or co-dispersal ofboth spores by means of seed plants from heterosporous pteridophytes tpro- the same vector (e.g., birds) (Taylor et aL 1993) gymnsperms),

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Pteridophyte Groups rangia lateral on the axes, Extant lycophytes include

the homosporous eligulate and the

Recent progress in molecular phytogeny (e.g.,heterosporous ligulate and Selaginella-

Hasebe et at. 1995, Pryer et al. 2001, 2004b, ceae. -This Schneider et al. 2004a, b) has accempanied redefi- Euplo,liqpdytes group is characterized nition of pteridophytic groups and proposal of new by the euphyllous or non-microphyllous leaves and groups (Fig, 1), Most of monophyletic and para- comprises monilophytes and seed plants, Euphylls phyletic groups below are the same as those of (true leaves) include fern megaphylls, seed plant Pryer et al. (2004b), and the phylogenetic relation- megaphylls, enation-like or ensiform reaves of ships ofmonophyletic groups are shown witli illus- Psilotaceae, and sphenophylls of Equisetaceae, trations by Pryer et al. (2004a), Monophyletic although they may have evolved recurrently in dii r groups sheuld be given appropriate taxonomic ranks ferent lineages. - tracheophytes to demonstrate phylogenetic relationships. lycophytes. Paraphyletic groups are not usable as taxonomic imnilophytes-This group comprises three units in a strict sense, but may be usefu1 in non-tax- free-sporing groups, i,e., ferns (which are not mono- onomic, general consideratien, representing evo- phyletic), Psilotaceae and Equisetaceae, the last

lutionary stages. two of which are conventionally separated as fern

allies, The monilophytes are sister to seed plants and Monopbyleticgroups defined by the euphylleus leaves (megaphylls or - 1]lolysporangiophytes This group comprises non- sphenophylls [in Psiiotum simple or fbrked ena- vascular and vascular plants with branched aerial tion-like], i.e,, non-microphyllous leaves) and

axes with multiple sporangia. Nonvascular members absence ofsecondary vascular tissue in addition to

have bryophytic hydroid- and leptoid-like conduct- pteridophytic reproduction. Monilophytes = euplry1- - ing cells and are known as fossils alone (e.g.,lophytes , - , Hbr:nopbyton), Polysporangiate plants Leptosporangiateforns Filicalean ferns with

are sister to nonvascular bryophytes with unbranch- leptosporangia that develop from single surface

ed, monosporangiate sporophytes, For the evolution cells ofmegaphyllous leaves. Osmundaceae, which

of polysporangiate branched axes see Kato & diverge the earliest among the leptosporangiate Akiyama (in press). ferns, show variable sporangium developmental 1>ueheophytes (vascularplants)LThis group patterns, part ofwhich is similar to the eusporangial is defined by having vascular tissues and cornprises pattern with a square-based archesporial celt, and the euphyllophytes and microphyllous lycophytes. It sporangia are massive and produce 128-512 spores,

"Rhyniopsida" also includes part of leafless (e.g.,an output intermediate between 1OOO or more in a Cboksonia) (Rothwell 1999, Pryer et al. 2004b). eusporangium and typically 64 in a leptosporangium Tracheophytes are a member of polysporangio- (Bower 1935). phytes and rnay be divided into eutracheophytes Aquaticforns (bydropteroicts)-This group and primitive tracheophytes, comprising Marsileaceae and Salviniaceae (usually lycopbytay (micmpby11Qpfp,tes)- [[his group is including Azollaceae) is deflned by the heterospory characterized by the microphyllous leaves with sin- and aquatic life form (Fig, IA), although the plants gle sporangia on the adaxial side of leaves or in vary so remarkably as to be sometimes classified at

the axil. It is sister to the euphyllophytes. The ances- the order or higher rank. Phylogenetically the aquat-

tral zosterophytes with nonleaf enations have spo- ic fems are not close to the heterosporous amphibi-

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August 20e5 KMO: Ptcridophyte phylogeny and evolution 123

ous Platyzoma (Pteridaceae),the same class level as fems. Different from mega- and to the homosperous aquatic fern Ceratopteris, phyllous ferns, they have non-megaphyllous leaves and are very remete from the heterosporous aquat- (microphylls in lycophytes, sphenophylls in

ic lsoetes of the microphyllous lycopods. Equisetaceae, and simple or fbrked enation-like or

Pblygrammoid.fernsrrThese ferns comprise ensifbrm leaves in Psilotaceae). The of the Polypodiaceae and Grammitidaceae, hence the name fern allies is shown by the phylogeny in which the is derived from a combination of the family names lycophytes are sister to the rest ofvascular plants, (Schneider et aL 2002). Grammitidaceae are sister to while Psilotaceae and Equisetaceae are assigned to Polypodium (R triseriale group) within Poly- the menilophytes. podiaceae (Fig. IB). The polygrammoids are epi- Eusporangiate.fl7rns-Megaphyllous ferns phytes with usually densely scaly, long-creeping with eusporangia that develop from multiple initial rhizomes and exindusiate discrete (round or elon- cells. Marattiaceae and Ophioglossaceae are such gate) sori superficial on the leafsurface. extant fems. The eusporangia are plesiomorphic, Lignophytes-This group comprises sper- possibly derived from those of the ancestral matophytes (seed plants) and pteridophytic pro- bryophytes, and shared by Psilotaceae, Equisetaceae, gymnosperms that are a free-sporing immediate seed plants, and lycophytes, i, e,, all vascular plants

ancestor, The shared or secondary vascular tis- except leptosporangiate fems. The last alone havc

sue is produced by the bifacial cambium and sup- derivative leptosporangia. ports arl)orescence, which is advantageous for light I thank H, Nozaki and M. N, famura who invited me to capture. It is likely that the progymnosperms ances- "Melocular the Symposium Phylogeny ofAsian Plants:' tral to seed plants were heterosporous, although I also thank C. Tsutsumi for reading the manuscript. DiMichele et al. (1989) assumed that they were This study was in part supported by a Grant-in-Aid for homosporous, Scientific Research from the Japan Society fbr the Promotion ef Science. Ptirap]tyleticgroups

Pteridbpbytes-These plants are free-sporing (non- References seed) vascular plants comprising fems, three fern Bateman, R. M. 1 996. Nonfioral homoplasy and evolu- allies belew). Among them, monilophytes (see tionary scenarios in living and fossil land plants. In Psilotaceae and Equisetaceae) are sister to (ferns, M. J. Sanderson & L. Huffbrd (eds.) Homoplasy, non-pteridophytic seed plants and together sister pp. 91-130. Academic Press, San Diego. - most to another ally, lycophytes. & W. A. DiMichele. 1994.Heterespory]the iter- ative kcy innovation in the evolutionary history ofthe IJlarnsmThis group with circinate, spore-bear- plant , BioL Rev. 69: 345-417. ing megaphyllous leavcs include eusporangiate and Beerling, D, J., C, P. Osborne & W, G. Chaloner. 2001. leptosporangiate ferns. The fems have convention- Evolution efleaf-form in land plants linked to atmos- ally treated as a single taxonomic been group, pheric C02 decline in the Late Palaeozoic era. Nature However, the eusporangiate Marattiaceae and 410: 352-354.

Bierhorst, D, W. 1977. The systematic of Ophioglossaceae form monophyletic groups along position Psilotutn and Tinesipteris. Brittonia 29i 3-13. with the fern allies Equisetaceae and Psilotaceae, Bower, F. O. 1935. Primitive Land Plants. Macmillan, respectively. London. fern allies-Thcse share free-spore repro- Chase, M. W., D. E. Soltis, R, G, Olmstcad, D. Morgan,

duction with ferns, Threc fern allies, lycophytes, D. H. Les, B. D. Mishler, M. R. Duvall, R. A. Pricc, Psilotacae and Equisetaceae, are often treated at H. G. Hills, Yl-L. Qiu, K. A. Kron, J. H. Rettig, E,

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Conti, J, D, Palmer, J, R. Manhart, K. J, Sytsma, H, horsetail Eeuisetum giganteum L. Bot. J. Linn. Soc. J. Michaels, W, J, Kress, K. G. Karol, W. D. Clark, 88: 11-34. M. Hedren, B. S. Gaut, R. K. Jansen, K.-J. Kim, C. F. Engler, A, & K., Prantl (cds.). 1902. Die NatUrlichen Wimpee, J, F, Smith, G. R. Fumier, S. H. Strauss, Q.- Pflanzenfamilienl(4). Pteridephyta. Velag non Y Xiang, G. M. Plunkett, R S, SoTtis, S, M, Swensen, Wilhelm Engelmann, Leipzig. S. E. Williams, P, A. Gadek, C, J, Quinn, L, E, Friedman, W. H. & M. E. Cook. 2000. The origin and Eguiarte, E, Golenberg, G. H. Learn, Jr., S. W. early evolution of tracheids in vascular plants: inte- Graham, S. C. H. Barrett, S. Dayanandan & V A. gration of palaeobotanical and beobotanical data, Albert. 1993, Phylogenetics of seed plants: an analy- Phil, Trans, R, Soc, London, B 355: 857-868. sis of nucleotide sequenc ¢ s from the plastid gene Hasebe, M., T. Omori, M. Nakazawa, T. Sano, M. Kato & rbcL, Ann, Missouri Bot, Gard. 89: 528-580. K. Iwatsuki. 1994, rbcL gene sequences provide Ching, R.-C. 1940, On natural elassification of the fami- evidencc for the evolutionary lineages ofleptospo-

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Received lanuary a 2005; accqpted March 23, 2005

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