Classification, Molecular Phylogeny ,Divergence Time, and Morphologic

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

Invitedarticle

Classification, Molecular Phylogeny,DivergenceTime, and MorphologicalEvolutionof Pteridophyteswith Notes on Heterospory and Monophyleticand Paraphyletic Groups MASAHIRO

KATO*

Department ofBiotogicat Sciences,Graduate Schoot ofScience, Universitv. Hongo, 7bk)]oIJ3of7bkyo, O033,lapan Pteridophytes are free-sporing vascular landplantsthatevolutionarily linkbryophytes and seed plants. Conventiona], hierarchic classifications ofptcridophytes using group (taxon)-based pheneticcharacters are briefiy reviewcd. Review isalso made forrecent trcc-basedcladistic analyses and molecular phylogenetic analyses with increasinglylarge datasets ofmultiplc genes(compared to single genes inprevious

studies)

and

increasinglylarge numbers

of spccies

to particulargroups inpreviousstudies), (compared

representing

itiscxtended

and

major

groupsof pteridophytes

to most recent analyses of esti-

divergcnce times ofpteridephytes, These c]assifications, phylogenetics, and divergcncc time estimates have improved our understanding of the diversity and historical structure of pteridophytes. Heterosporyisnoted with referencc to itsorigins, endospory, fertilization, and dispersal. Finally, mating

menophylctic

Key

words:

and

paraphyletic groupsrccently

classification,

divergencetimc

proposed

estimate.

or re-recognized

briefly dcscribcd.

fems,heterospory, molecular

dophytcs.

Morphological Classifications

are

phylogcny,pteri-

diversification, resulting in a total of about 12,OOOspecies, which may be primitive or advanced. The species were classified in many difl Pteridophytes, likeseed plants(gymnosperms and ferentclassificatien systems basedon morphologiangiosperms), are vascular landplants and also are similar to nonvascular bryophytes inthefree-speringcal characters. Some of major classifications put reproduction, Evolutionarily they fo11owedbryo- fbrwardinthe 20th century are brieflynoted here Thus, free-sporing phytes and precededseed plants.

it a

recent

1, 2). ('lables

Engler & Prantl(1902) classified pteridophytes in a broad sense plantsor pteridophytes havea long(420million years)evolutionary histo- into fbur classes, Filicales,Sphenophyllales, Equisetales and fycopodia]es, and subdivided the ry, and on the other hand,likeangiosperms, exhibvascular

*

PTesent address: Departmentof Botany,NationalScienceMuseum, Tsukuba 305-OO05,Japan

e-mail

address,

[email protected]

Thisarticle isfonnedfremthepresentation as one of contributions forthe International Symposium 2004, Asian Plant Systematics, heldat Sakura,Chiba,Japanon July29 August 2,2004,

Diversity and

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1.Classifications ofmajoT ptcridophytc groups proposed by sorne among grouping in each classification and do not correspond

TABLE

cate

basedon

authors,

cemparative

morphology,

Numbers indi-

classifications.

Engler& PranttC1902)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]ales 1-1.Se]agine]]ales

1-1.Selaginel[ales 1-1.SeiaginellRlesl-1,Selaginellales 1-1,Selaginellales

1-I-2.Isoetineae

1-2,Jsoetales

l-2.Isoetales

1-2.Isoetales

1-2.Lycopodia]cs]-2,Isoctales

1-2,lsoetales

1-2.Eligulatae

3,Equisetopsida

2.Isocphytina1-3.Lycopodiales1-3,Lycepodiales 3,Psjophytina 2.Psilotatae 3.Sphenophytina 4,Sphenophytina 2.Equisetopsida 3.Equisetatae

4.Pteropsida

4.Filicophytina

1-2-1.LycopDdincac

1-3.Lycopodia]es1-3.Lycopodiales

1-2-2.Psilotineae

2.Psi]ophytinae 2,Psi]opsida

2.Equiestales

3.Articulatae

1-3.Lycopodjales

2,?sjophytina

3,SphenophylLates 4.Filica]es

4.Filicinae

5.Fi]icophytina3.Fiticopsida

4.Filicatae

(incl.Psilotaceae) Extinctgroup included inEquisetopsidain other

classifications,

2.Classifications ofmajor ferngroupsproposedby some authors,based on comparative morphology. Numbers indicate groupingin each classification and do not correspond among classifications.

TABi.E

Christellsen(l938)Cepeland(1947)Tagawa&iwatsuki(1972)PichiSermolli(1977)Ching{IY7S)

Tryon&Tryen(1982)

1,Eusporangiatae

1.Eusporangiopsida

1,Polypodiidae

1-].Ophioglossales

].Qphioglossales 1.0phioglossales

1,Ophioglossopsida

1-1,Ophioglossales

1-1.0phioglossales

1-2,Maradiaies

2.Marattiales

2.Maraniales

2.Marattiepsida

1-2.Marattia]es

1-2.Marattiales

3.Filicales

3,Fllicopsida

2,Protoleptosporangiopsida1-3.PojypodiaLes

3-].Osmundjclae

3.Leptosporangiopsida t-3-1.Po]ypodiineae

3-2,Plagiogyriidae

3-t,Po]ypodiales

2,Leptosporangiatae 3.FiHcales 2-1.Filicales

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

intotal 14 families including the Iargefamily rangiatae Eufilicineae and HydroPolypodiaceae with 15 subfamilies. Ching (1940) (suborders Maiattiales and Ophioglossales, and the classified into33 families and recpteridineae), class Lycopodiales intotwo orders Lycopodiales ognized fiveseries 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, 1913Pteridophyta) into fivesubdivisions: subdiv, 1934) Index Filicum and supplements I-IIIenuLycophytina comprising orders Lycopodiales and merated all fernspecies ofthe world described, In SeJaginellales, threemonotypic subdiv, Isoephytina, his systematic classification of fernsChristensen Sphenophytina and Psilophytina,and subdiv. recognized two series (Filices EusporangiataeFilicophytina comprising three classes (Eusporan(1938) and FilicesLeptosporangiatae),two orders Ophioglossales and Marattiales], giopsida [orders Ophioglossales and Marattiales intheformerseries Protoleptosporangiopsida [Osmundales], and and two orders Filicales and Salviniales inthe latteg Leptosporangiopsida [Polypodiales or Filicales, class

Filicales intothree orders, Filicalesleptospo-

and

"Polypodiaceae"

"Poly-

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evelution

Polypodiineae,Marsileineae,and (suborders Copeland(1 947)recognized orders Ophioglossales Salviniineae), and dividedLycopodiopsida into Marattiales and Filicales Selaginellales and Isoetalcs. Ttyon & (1family), (1family), (19 bycopodiales, families including Marsileaceaeand Salviniaceae), Tryon (1982) included Psilotaceae in Filicopsida Holttum (1949) classified leptosporangiate ferns (ferns) based on BierhorsVs (1977and references into14 families including the largefamilyDenncited therein) morphological and anatomical results staedtiaceae with 11 subfamilies and proposed three and spore wall characters. ofwhich one isterrninated by In short, the classifications basedon phenetic phylegeneticlineages, rlagawa Dennstaedtiaceae. & Iwatsuki(1972) adoptcharacters usually recognized four major groups ed the conventional classificationofpteridophytes of living which fernswere pteridophytes,among intofourclasses Psiopsida, Lycopsida,Equiset- divided intoMarattiales, Ophioglossalesand opsida, and Pteropsida. They classjfied Pteropsida Filicales, although certain groups(e.g., Psilotaceae intoerders Ophioglossales, Marattiales,Filicalcs, and aquatic ferns) were assigned to different groups Marsileales,and Salviniales.[lagawa & Iwatsuki ofhigher ranks or treatedat different ranks ([lables recognized intotal34 families forpterido- 1,2).Characters that are infbrmative throughout (1972) PichiSermolli classified phytes of Thailand. (1977) pteridophytesare not many. Those classifications Pteridophytaintofbursubdivisions, Lycophytina, with hierarchic ranks are generally taxon-based and Sphenophytina,Psilophytina,and Filicophytina, have usually not been given statistically analyzed The firstthree were monotypic each with single interrelationships of families. classes,while the last Filicophytina comprised three classes, Ophioglossopsida,Marattiopsida and Molecular Phylogenies Marsileales, Salviniales]).In Genera Filicum

Filicopsida. PichiSermolli(1977) assigned

58

of64

familiesto Filicopsida, 3 to Lycopsida, 1 to

Achievementofmelecular phylogeny,which isdisEquisetopsida,and 2 to Psilotopsida.Kramer & tree,succeeded longconplayedas a phylegenetic Green (1990) compiled contributions to pterido- tributionsof systematics, classifications, and fioras basedon pheneticor morphological characters, phyteclassificationand presenteda similar classification system of fourclasses Psilotatae (1family), as noted above, Molecular analyses with largedata Lycopodiatae (3families), Equisetatae(1 family), sets dealingwith all or most pteridophyte groups and Filicatae(33families).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 largedata and Pteridaceae; treefernfamilies; Lomariopsidaset (ca, 500 operational taxonomic units), Hasebe et ceae, Davalliaceae,Nephrolepidaceae, Oleandra- aL (1994) presenteda molecular phylogeny oflepceae and Dryopteridaceae; Polypodiaceae and tosporangiateferns deducedfromrbcL sequences of Grarmnitidaceae; and Azollaceae and Salviniaceae.58 species representing almost all farnilies recogTryon & Tryon (1982)divided Division nized inthe then classifications (Kramer & Green Pteridophyta intothree classes Filicopsida, 1990).The number of familiesthey dealtwith was Equisetopsida(with a single Lycopodiopsida, and two subclasses

order

subdivided

Equisetales)and

1argerthan that of

Filieopsidainto

although the number

Po]ypodiidae and Psilotidae. Tryon

& Tryon (1982) further dividedPolypodiidae into orders

Ctphioglossales, Marattiales, and Polypodiales

any

molecular analyses, previous of species per family was few.

Hasebe et al,'s (1994) pioneerwork

solved

several

on pteridophyte questions phylogeny accelerated research to solve them, One of their

of significant and

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Clade4

kgg=uttsE MarsileaRegnellidium

n=ep-oEEege'opt

PilulariaAzollaSalvinia Clade3

Clade2Clade 1Davalliaceae

if4s,¢yueheophytes (vascularplants)LThis group

patterns, partofwhich issimilar to the eusporangial isdefinedby having vascular tissues and cornprises witha square-based archesporial celt,and the pattern euphyllophytes and microphyllous lycophytes. It sporangia are massive and produce128-512spores, also includes between1OOO or more ina partof leafless (e.g.,an output intermediate Cboksonia) (Rothwell 1999, Pryer et al. 2004b). eusporangium and typically 64 ina leptosporangium Tracheophytesare a member of polysporangio(Bower1935). Aquaticforns(bydropteroicts)-This phytesand rnay be dividedintoeutracheophytes group "Rhyniopsida"

and

primitivetracheophytes,

comprising

[[hisgroupis lycopbytay (micmpby11Qpfp,tes)characterized

by the microphyllous

leaveswith sin-

gle sporangia on the adaxial side of leavesor in theaxil. Itissister to theeuphyllophytes. The ancestralzosterophytes

with

nonleaf

enations

havespo-

Marsileaceaeand Salviniaceae(usually

including Azollaceae)isdeflned by theheterospory and aquatic lifeform (Fig, IA),although theplants vary so remarkably as to be sometimes classified at theorder or higherrank. Phylogenetically theaquat-

icfemsare not close to theheterosporous amphibi-

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evolution

levelas fems.Differentfrommegaand to thehomosperousaquatic fernCeratopteris, phyllous ferns, they havenon-megaphyllous leaves in and are very remete from the heterosporous aquatin lycophytes,sphenophylls (microphylls iclsoetesof the microphyllous lycopods. Equisetaceae,and simple or fbrkedenation-like or Pblygrammoid.fernsrrThese fernscomprise ensifbrm leavesinPsilotaceae). The paraphylyof the Polypodiaceae and Grammitidaceae, hencethename fernalliesis shown by the phylogenyin which the isderivedfrom a combination of the family names lycophytes are sisterto the rest ofvascular plants, et aL 2002). Grammitidaceae are sister to while Psilotaceae and Equisetaceae are assigned to (Schneider ous

leptosporangiate fernPlatyzoma

Ptcridophytephylogeny

(R

Polypodium

the same (Pteridaceae),

Poly-

triseriale group) within

class

the menilophytes.

IB). The polygrammoidsare epiEusporangiate.fl7rns-Megaphyllous ferns podiaceae(Fig. phyteswith usually denselyscaly, long-creeping with eusporangia thatdevelopfrom multiple initial rhizomes and exindusiate discrete or eloncells. Marattiaceae and Ophioglossaceae are such (round extant fems.The eusporangia are plesiomorphic, gate)sori superficial on the leafsurface. Lignophytes-This

possibly derived from those of the ancestral Equisetaceae, matophytes and shared by Psilotaceae, (seed plants)and pteridophyticpro- bryophytes, immediate seed plants,and lycophytes, i,e,, all vascular plants gymnosperms that are a free-sporing ancestor, The shared wood or secondary vascular tis- except leptosporangiate fems.The lastalone havc sue isproduced by the bifacial cambium and supderivative leptosporangia. portsarl)orescence, capture.

tralto

which

group comprises

isadvantageous

sper-

forlight

Itis likelythat the progymnospermsancesseed

DiMichele

plants were et al.

heterosporous, although

(1989)assumed

that they were

homosporous,

I thank H, Nozaki and M. N, famura who invited me to the Symposium "Melocular PhylogenyofAsian Plants:' I also thank C. Tsutsumi forreading the manuscript. This study was in partsupported by a Grant-in-Aid for Scientific Research from the Japan Societyfbrthe Promotionef Science.

Ptirap]tyleticgroups

Pteridbpbytes-These References plantsare free-sporing (nonseed) vascular plants comprising fems,three fern Bateman, R. M. 1 996.Nonfioral homoplasy and evoluallies (see belew).Among them, monilophytes tionary scenarios in living and fossil landplants.In Psilotaceaeand (ferns,

sister

to

plantsand together sister ally, lycophytes.

non-pteridophytic

to another

Equisetaceae)are

seed

IJlarnsmThisgroup with

ingmegaphyllous

circinate,

spore-bear-

leavcsincludeeusporangiate

and

leptosporangiateferns.The fems have conventionally

been treatedas

a single

taxonomic group,

However, the eusporangiate Marattiaceaeand Ophioglossaceae form monophyletic groups along with the fernallies Equisetaceaeand Psilotaceae,

M. J. Sanderson& L. Huffbrd(eds.) Homoplasy, pp. 91-130.Academic Press,San Diego. - & W. A. DiMichele. 1994.Heterespory] the most iterative kcy innovation intheevolutionary history ofthe kingdom, BioL Rev. 69: 345-417. plant Beerling, D, J.,C, P.Osborne & W, G. Chaloner. 2001. linkedto atmosEvolution efleaf-form in land plants phericC02 declinein the Late Palaeozoicera. Nature 410: 352-354. Bierhorst, D, W.

1977. The

systematic

position

of

Psilotutn and Tinesipteris. Brittonia 29i3-13. Bower, F. O. 1935.PrimitiveLand Plants.Macmillan, respectively. London. fern allies-Thcse share free-spore reproChase,M. W., D. E. Soltis, R, G, Olmstcad,D. Morgan, ductionwith ferns,Threc fernallies, lycophytes, D. H. Les,B. D. Mishler, M. R. Duvall,R. A. Pricc, Psilotacaeand 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, J.Michaels, W, J,Kress,K. G. Karol,W. D. Clark, M. Hedren, B. S.Gaut,R. K. Jansen,K.-J.Kim, C. F. Wimpee,J,F,Smith,G. R. Fumier,S. H. Strauss, Q.Y Xiang,G. M. Plunkett, R S, SoTtis, S,M, Swensen, S. E. Williams,P, A. Gadek, C, J, Quinn, L, E, Eguiarte,E, Golenberg, G. H. Learn, Jr.,S. W. Graham, S. C. H. Barrett, S. Dayanandan & V A. Albert.1993,Phylogenetics of seed plants: an analysis of nucleotide sequenc ¢ s from the plastid gene rbcL, Ann, MissouriBot,Gard. 89:528-580. Ching,R.-C.1940,On natural elassification of the family Sunyatsenia 5:201-268. . 1978. The Chinese fernfamiliesand gencra:systematic arrangement and historical origin. Acta Phytotax.Sin.16:1-19. Christensen, C, 1905,IndexFilicum.Hafhiae.1973 ed. Koeltz,Koenigstein, , 1913-1934. Index Filicum,Supplementum i-III Hafuiae. 1973 ed. Keeltz,Koenigstein.