Classification, Molecular Phylogeny, Divergence Time, and Morphological Evolution of Pteridophytes with Notes on Heterospory and Monophyletic and Paraphyletic Groups

2005·1.5 MB·English

by  Kato, Masahiro

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

Invited
article
ClassificatiMoolne,cularPhylogeny,DivergenceTime,
and
Morphological Evolution of Pteridophyte swith Notes on Heterospory
Monophyletic ParaphyleticGroups
and and
MASAHIRO KATO*

DepartmentofBiotogiScciaetnces,GraduatSechootofSciencUeni,versitovf.7bkyHoo,ngo,7bk)]oIJ3-

O033,lapan

Pteridophyt earse free-spori vnagscular land plants tha tevolutionarily lin kbryophyt eansd seed plants.
Conventiona ]g,roup (taxon)-b haisereadrch iclcassifications ofptcridophytes using pheneti ccharacters
are briefi ryeviewcd. Review is also made for recent trcc-based cladistic analyses and molecular phy-
logeneti acnalyses with increasingl ylarg edata sets ofmultiplc genes (compar teod single genes in pre-
vious studies) and increasingly large numbers of spccies representing major groups of pteridophytes
(compar teod particula rgroups in previou sstudies), and it is cxtended to most recent analyses of esti-
mating divergcnc teimes ofpteridephytes, These c]assifications, phylogeneti casnd, divergcnc tcime esti-
mates have improved our understanding of the diversi taynd historic astlructure of pteridophytes.
Heterospor yis noted with referencc to it sorigins, endospory, fertiliza tanido nd,ispersa lF.inally,
menophylctic and paraphylet igcroups rccently proposed or re-recognized are brief dlcyscribcd.
Key words: classification, divergenc etimc estimate. fems,heterospor ymo,lecular phylogcny ,pteri-
dophytcs.
Morphological Classifications it a recent diversificat ireosnul,ting in a total of
about 12,OO Ospecies, which may be primitiv oer
Pteridophytes l,ik eseed plant s(gymnospe ranmds advanced. The species were classified in many difl
angiosperms), are vascular land plant sand also are feren tclassificatien systems based on morphologi-
similar to nonvascular bryophyte isn the free-speringcal characters. Some of major classifications put
reproduction, Evolutionar itlhyey fo11owe dbryo- fbrward in the 20th century are briefl ynoted here
phytes and precede dseed plant sT.hus, free-sporing ('lab l1e, s2).
vascular plant sor pteridophyt eisn a broad sense Engler & Prant l(190 2cl)assified pteridophytes
have a long (42 0million years) evolutionary histo- into fbur classes, Filicales ,Sphenophyllales,
ry, and on the other hand, lik eangiosperms, exhib- Equisetal eansd fycopodia a]ndes s,ubdivided the
* PTesent address: Department of Botany ,Nationa lScienc eMuseum, Tsukuba 305-OO05, Japan e-mail address,
[email protected]
This article is fonne dfrem the presentati aosn one of contributions for the Internatio nSaylmposium 2004, Asian Plant
Diversity and Systematic sh,eld at Sakura ,Chiba, Japan on July 29 - August 2, 2004,
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TABLE 1 . Classificati oonfmsajoT ptcridophytc groups proposed by sorne authors, base don cemparative morphology, Numbers indi-
cate grouping in each classification and do not correspond among classifications.
Engler& PranttC1902)Verdooun(1938)Tagawa&Iwatsuki(1972)PichiSermolli(1977)Chmg{E97S)Tr&yToTn)'on(1982Kr)arner& Green(1990)

1,Lycopodiales 1,Lycopodiina e 1.Lycopsida 1.Lycephytina 1,Lycephytina1.Lycoodiepsida 1.Lycopodiatae
1-1.Ligulatae
1-1-t.Se]aginellineae1-1.Selaginel]al1e-s1.Se]agine]]ales 1-1.Selaginel[ales1-1.SeiaginellRlesl-1,Selaginellal1e-s1,Selaginellales
1-I-2.Isoetineae l-2.Isoetales 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.Isocphytina1-3.Lycopodiales1-3,Lycepodiales

1-2-2.Psilotineae 2.Psi]ophytinae2,Psi]opsida 2,?sjophytina 3,Psjophytina 2.Psilotatae
2.Equiestales 3.Articulatae 3,Equisetopsida 3.Sphenophytina4,Sphenophyti2n.aEquisetopsida 3.Equisetatae

3,SphenophylLates
4.Filica]es 4. Filicinae 4.Pteropsida 4.Filicophytina 5.Fi]icophytina3.Fiticopsida 4.Filicatae
(incl.Psilotaceae)
Extinc tgroup includ eidn Equisetopsid ain other classifications,
TABi.E 2. Classificati oofnmsajor fer ngroups proposed by some authors, based on comparative morphology. Numbers indicat geroup-
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 ].Qphioglossa1l.0epshioglossales 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,Leptosporangiat3a. eFiHcales 3.Filicales 3,Fllicopsida 2,Protoleptosporangiopsida1-3.PojypodiaLes
2-1.Filicales 3-].Osmundjclae 3.Leptosporangiopsidat-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 Filical eisnt othree orders, Filicale sleptospo- and in total 14 familie isncludin tghe Iarge family
rangiatae (suborde rEsufilicineae and Hydro- Polypodiaceae with 15 subfamilies. Ching (1940)
pteridine aMea)i,attiale asnd Ophioglossale sa,nd the classified "Polypodiaceae" int o33 famili easnd rec-
class Lycopodiale isnto two orders Lycopodiales ognized fiv eseries in the polyphyletic "Poly-
eligulatae including suborder Psilotinea eand podiaceae" in the context of phylogeny, Ching
Lycepodiale lsigulat awieth suborders Selaginetli-(197 8c)lassified Chinese pteridophyt e(sdivision
neae and Isoetineae ,Christensen' s(190 51,913- Pteridophyta) into fiv esubdivisions: subdiv,
1934) Index Filicum and supplements I-II Ienu- Lycophytina comprising orders Lycopodiale sand
fern describedI,n SeJaginellaltehsr,ee Isoephytina,
merated all species ofthe world monotypic subdiv,
his systematic classification of fern sChristensen Sphenophytina and Psilophytina ,and subdiv.
(193 r8ec)ognized two series (Fil iEucsepsorangiataeFilicophyti cnoamprising three classes (Eusporan-
and Filice sLeptosporangiatae) ,two orders giopsida [orde Orpshioglossal eansd Marattiales],
Ophioglossal aensd Marattial eisn the former series Protoleptosporangiopsida [Osmundales ]a,nd
and two orders Filicale asnd Salvinia lien sthe latteg Leptosporangiopsida [Polypodi aorl eFislicales,
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Marsileales, Salviniales]) .In Genera Filicum (suborde Proslypodiineae ,Marsileineae ,and
Copeland ( 1947) recognized orders Ophioglossales Salviniinea ea)nd, divide dLycopodiopsida into
(1 family )M,arattial e(s 1family )a,nd Filicale (s19 bycopodia Sleelasg,inellal eansd Isoetalc sT.tyon &
familie isncludin Mgarsileaceae and Salviniaceae), Tryon (1982 i)ncluded Psilotace aien Filicopsida
Holttum (1949 c)lassified leptosporangi afteerns (fern bsa)sed on BierhorsV (s197 7and references
int o14 familie isncludin tghe larg efamil yDenn- cited therei nmo)rphological and anatomical results
staedtiaceae with 1 1 subfamilies and proposed three and spore wall characters.
phylegeneti clineage osf,which one is terrninated by In short, the classifications based on phenetic
rlagawa
Dennstaedtiacea e. & Iwatsuki (197 2ad)opt- characters usually recognized four major groups
ed the conventional classification ofpteridophytes of livin gpteridophytes ,among which fern swere
int ofour classes Psiopsid aL,ycopsida ,Equiset- divided into Marattiale sO,phioglossale sand
opsida, and Pteropsid aT.hey classjfied Pteropsida Filicale sa,lthough certain groups (e. gP.si,lotaceae
int oerders Ophioglossale Msa,rattiales ,Filicalcs, and aquatic ferns w)ere assigned to differe gnrtoups
Marsileales ,and Salviniales .[lagawa & Iwatsuki ofhigher ranks or treate dat differe nratnks ([lables
(1972 r)ecognized in tota l34 familie fsor pterido- 1, 2). Character tshat are infbrmati vtehroughout
phytes of Thailand P.ichi Sermoll (i197 7cl)assified pteridophyte sare not many. Those classifications
Pteridophyta int ofbur subdivisions, Lycophytina, with hierarchi rcanks are general ltyaxon-based and
Sphenophytina ,Psilophytina ,and Filicophytina, have usually not been given statistically analyzed
The firs tthree were monotypic each with single interrelations ohfi pfsamilies.
classes, while the las tFilicophyt iconmaprised three
classes, Ophioglossopsida ,Marattiopsida and Molecular Phylogenies
Filicopsid aP.ichi Sermolli (197 7as)signed 58 of64
familie sto Filicopsida, 3 to Lycopsida, 1 to Achievemen tofmelecular phylogeny, which is dis-
Equisetopsida ,and 2 to Psilotopsida .Kramer & played as a phylegenet itcree ,succeeded long con-
Green (1990 c)ompiled contributions to pterido- tribution sof systematics, classifications, and fio-
phyte classification and presented a similar classi- ras based on phenetic or morphological characters,
ficati osynstem of four classes Psilotata (e1 family), as noted above, Molecular analyses with large data
Lycopodiatae (3 families E)q,uisetata e(1 family), sets dealing with all or most pteridophy tgeroups
and Filicata e(33 families) .Among families of have been explosive since the middle 1990s. One
Filicatae ,affinities were suggested between year late trhan Chase et al.'s (1993 ep)och-making
Dipteridace aaned Cheiropleuriace aVei;ttariaceaestudy on angiosperm phylogeny using a larg edata
and Pteridacea ter;ee fern familie sLo;mariopsida- set (ca 5,00 operational taxonomic units), Hasebe et
ceae, Davalliaceae ,Nephrolepidacea eO,leandra- aL (1994 p)resented a molecular phylogeny oflep-
ceae and Dryopteridaceae; Polypodiaceae and tosporangiat efern sdeduced from rbcL sequences of
Grarmnitidaceae;Azollaceae Salviniaceae.58 farnilies
and and species representing almost all recog-
Tryon & Tryon (1982 )divided Division nized in the then classifications (Krame &r Green
Pteridophyta into three classes Filicopsida, 1990). The number of familie sthey dealt with was
Equisetopsida (wit ha single order Equisetales )and 1arge rthan that of any previou msolecular analyses,
Lycopodiopsida, and subdivided Filieopsid ainto although the number of species per famil ywas few.
two subclasses Po]ypodiidae and Psilotid aTer.yon Hasebe et al,'s (199 4pi)onee rwork solved several
& Tryon (1982 f)urthe drivide dPolypodiidae into of significant question osn pteridophy tpehylogeny
orders Ctphioglossal eMsa,rattiale sa,nd Polypodiales and accelerated research to solve them, One of their
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FiG .1. Monophyletic and paraphylet igcroups ofpteridophytes. A. Monophyletjc aquatic ferns A.iolta and Satvini aare assigned to
Salviniaceae or each genus t,o monotypic family .Tree is adapted from Pryer (1999 )B.. Monophyly of Polypediaceae and
Grammitidacea e(polygrarnm aondi dthsat) ofepiphytic polygrammoid fern sand Davalliacea eF.our clades ofpolygrammotd fenis
are defin ebdy Schneide ert at, (2004b )S.elid triangl icn clade 4 indicat Gersammitidaceae. C. Majer greups ef polysperan-
giophytes G.roups on the right side are monophyletic, and groups en the top are paraphyleti cP.rotracheophyte msay be para-
phylcti cP.art ofdrawing is modified from Pryer et al. (2004b).
finding iss that feim sthat were considered primitive or apical annulus. The sporangium of Hymeno-
by morphological systematics diverg eearlier than phyllacea eand Gleicheniace haaes an oblique annu-
morphologically more advanced groups .For exam- lus ,while highe rleptosporangi faetren shave small,
ple, Osmundaceae are the basalmos tin leptospo- flattene sdporangia with vertical annuli. It is hypoth-
rangiate ferns ,and Hymenophyllaceae and a group esized that the sporangium morphology evo]ved
of Gleicheniacea eD,ipteridacea e(al sCoheiro- from a massive to small capsule and from the dista1
pleuriaceae )and Matoniacea eare the second and to oblique and then to vertical annulus (Bower
thir dbasa] I,n comparison, Vittariacea eP,teridaceae, l935).
Polypodiacea eD,avalliacea Der,yopteridace aaend, The second of their finding iss that tree fern
seme others are branche d1ate Tzhis order ofbranch- familie sC,yatheacea eD,icksoniaceae and Metaxy-
ing is in good accordance with the polari tofy trend aceae, along with Plagiogyriaceae, are mono-
of sporangia. The sporangium of Osmundaceae is phyletic ,although Plagiogyriace aaree not typical-
massive and, along with Schizaeaceae ,has a laterally tree ferns T.raditionall tyh,e two tree fer nfamilies
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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 Grammitidacea ehave free venation and aci-
Dicksoniaceaeb,yhavinghairs hairsbesides Later,
sori, and and mar- cular scales, a multigene phy-
gina lsori. Metaxyaceae, like Plagiogyriacea es,how logeneti canalysis with much ]arge rdata sets shows
a combination of hair appendages and superficial that Gramrnitidaceae are nested within Polypodia-
sori (soenos oRrecie)n,tl yH,ymenophyllopsidaceae,ceae and the two famili earse togethe rcoined "poly-
a small nontree fern family endemic to the grarnmoid "fern s(Schnei dete arl. 2002, 2004b),
Venezuelan Guayana, Guyana and Brazilia nsand- Furthermore, this polygrammoid group and
stone highland s(tepu iwesre), unraveled to have a Davalliace adeiffe irn that the sori are marginal and
close relationship with the tree fer ngroup (Wblfetindusia tien Davalliaceae and superficial and exin-
al. 1999) .It supports monophyly ofthe tree fer nand dusiat ein the polygrammoid group. Comparison
related nontree fern familie sH.ence, this tree-fern with their successive sisters (e,g .Ol,eandra,
clade saw marked evolutienary changes in stern AJI?phrolepi san,d Arthrqpteris )indicat etshat the
habit ,dermal appendage, lamina histolog yso,ral 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 finding iss wonhy densel yscaly, long-creepi ndgo,rsivent rT`ahlizornes
of special mention. It is that the aquatic and het- (bu tthe rhizomes are short and the leave sare radi-
erosporous fer nfamilies ,Azollacea eM,arsileaceae,ally arranged in many Grammitidaceae )a, com-
Salviniaceafeb,rm (Fig. dictyostelic
and a mQnophyletic clade plex vascular system ofthe rhizome, and
1A). Aquatic lif eand heterospor ayre usually con- epiphytism. Davalliaceae and the polygrammoids,
sidered to be a curiously enough sharing, because lik eVittariace aaree, typical epjphytic fer nfamilies.
the familie sare so distin citn the vegetative and The monophyly suggests the origin ofthe epiphyt-
reproductive characters as to be place ddistant iory ic famili efsrom a common ancestor of a certain life
ctassified at higher ranks in traditien acllassifica- form,
tions ,as noted above. Rothwel l& Stockey (1994) Phylogenet iacnalyses using increasingl ylarge
discovere da fossi lfern ,Ilydmpteris, and inter- data sets in the number of groups and the lengt hof
prete dthat it has intermediat meorphologies between DNA sequences fbllowed. Hasebe et aL7s (1995)
Marsileaceae and Salviniacea eR.othwell & Stockey analysis with more species Emd famili ethsan Hasebe
(1994 r)ecognized the order Hydropteridal ceosm- et al. (199 4pr)esented simjlar results. In an analy-
prisin gthe fossi Ill}pdmpteri asnd the extant Azolla- sis with 35 species of fern sand fern allies (i.e.,
Marsileaceae SalviniaceaeH.asebe lycophytesE,guisetum, Psilotaceae)
ceae, and et and and mul-
al.'s (1994 m)olecular evidence is in good accor- tiple genes (thre cehloroplast genes and a nuclear
dance with Rothwell & Stockey's (199 t4re)atment gene) ,Pryer et al. (200 1fb)und noteworthy rela-
of the aquatic fern farnili eMso.nophyly of the tionship sof lower pteridophytes .Tracheophytes
aquatic fern sis also supported by a combined mol- diverg efir sitnt othe rnicrophyllous lycophyte asnd
ecular and morphological analysis (Pry e1r999), the euphyllous plant s(Fi g1C.). This divergenc ies
The combination of aquatic lif eand heterospory in fu1 1agreement with the one that had been pro-
will be discusse bdelow. posed from the chloroplast gene order (Raubes &on
The fburt hof their finding iss monephyly of Jansen 1992) ,The euphyllous plants diverg einto
Polypodiaceae, Grammitidaceae and Davalliaceae seed plants and euphyllous pteridophytes called
(Fi gIB.) .Polypodiaceae and Grammitidaceae difl monilophytes. The monilophytes in turn comprise
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euspQrangiate and leptosporangiate ferns, Because those differenc aeres equally larg ebetween
Psilotacea ean,d Equisetum .Psilotace afebrm a the fbur groups ,the pteridophyt ewesre usually
clade with the eusporangiate Qphioglossa wcheialee,classified on the class level O,phioglossaceae are
Eguisetum fbrms another clade with the eusporan- morphologically more similar te other megaphyllous
giat eMarattiace atehough support is low, fems than to Psilotacea aelt,hough molecular evi-
Pryer et al, (2004 bex)tended their analysis dence suggests monophyly, The most conspicuous
fbr 62 taxa, using the same four genes ,and con- differen bceetween Ophioglossace aaned Psilotaceae
stmcted almos tthe same phylogenet itrcee as that of is the presence or absence of the root, but it is
Pryer et aL (200 1al)th,ough ther eis a differen cien uncertain whether the root was los tin Psilotacea eor
the positio nof Gleicheniacea Mea,toniacea eand i tnever appeared at the appearance ofthe family I.t
Dipteridace a(einclud Cihneigropleuriace aAef)te.r is the case with Equisetum. The larges dtifference
the divergenc eof 0smundaceae, the rest of lep- from Marattiaceae is seen in the reproductive organ
tosporangiate ferns divide sinto Hymenophyllaceae and phyllotaxis I.t is hypothesize tdhat the sporan-
and all others in Pryer et aL's (200 1tr)ee ,whereas in giophorous strobilus and whor]ed leaMe sappeared in
Pryer et al.'s (2004 bt)ree a monophyletic group the early divergenc eof Equisetopsid aT.hus, the
of Hymenophyllaceae along with Gleicheniaceae, molecular phylegeny suggests that remarkal)le mor-
Matoniacea eand Dipteridace adeiverge fsrom the phologic adliversifica tmaiyon have occurred in the
remaining of ferns .Matoniaceae diffe rfrom the early evolution of the basa leuphyllous pterido-
sister-group Dipteridaceae in that the former have phytes.
discre tiendusia tseori and the latte rhave acrosti-
(i.e. DivergenceTime
choid exindusiate sori sporangia are scattered),
although they share hair s(scal aebssent). The phy-
logen ythat the exindusiate Gleicheniacea eare like- As molecular data haye been accumulated fbr pteri-
ly sister to the Matoniaceae-Dipteridaceae clade dophyte phylogeny ,analyses with large data sets
(Hase bete al. 1995, Pryer et al. 2004b) supports that have been extending to estimating the divergence
the extant and fossi Mlatoniacea ewith peltat iendu- times ofmajor groups ofpteridophytes, In penalized
sia were deriye dfrom exindusiate members of the likelyhoo danalyses of fern sand angiosperms,
famil y(Kat &o Setoguch i1999). Schneider et al. (2004 ad)emonstrated that most
The above results show sharp conflict to the polypodioi (di an broad sense) or higher leptospo-
traditional classifications of pteridophyt ebsased rangiate fern sdiversifi iend the Cretaceou s(100
on comparative motphology, with special reference Mya or late rM;ya = million years ago) after angio-
to Iower groups. Previousl yp,teridophyt ewsere sperm radiation. They furthe srttggested that the
usually classified int ofern (sFilicop asndi tdhare)e fern diversifica twaison an ecological opportunistic
classes of fern allies, i.e P.siopsida ,Lycopsida, and response to the diversifica tofio anngiosperms, as
Equisetepsi d(aFi gI.C). The Lycopsid ais defined angiosperms came to dominate terrestri aeclosys-
by the monosporangiate microphyllous leaves. tems. Recently a,n unconventional photoreceptor
Psiopsid ais characterized by the absence of roots phytochrome 3 was discovere din a polypodioid
and typica lleaves w,hile Equisetopsida is charac- fern ,Adiantum pedatum (Kawa iet al, 2003).
terized by the strobilus comprising sporangjophores Phytochreme 3 functio nfsor red-light-induced pho-
with inwardl yoriented sporangia and the whorled totropism and for red-light-induced chlorop]ast pho-
sphenophylls. Filicopsid ahas megaphyllous leaves torc]ocatio nt,hereby conferring a distin cadtvantage
bearing aggregates of sporangia (call esodri). under low-lig hcatnopy conditions. Schneider et aL
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(2004 aarg)ued that the photorecept woars involved logica lchanges between O. cinnamomea and O.
in the diversifica tofio fnern sin angiosperrn-domj- claytoniana since the earliest diyergenc eof the
nant dense fores etcospaces. extant Osmundaceae, as also shown by foss ielvi-
A similar divergenc teime estimate, together dence (Trias Os. icdcytoniites). Yatabe et aL (1999)
with molecular phylogeny w)as undertaken for basal estimated the divergenc etime to be 294 or 322
fems (Pry eet ral. 2004b) .Using penalized likeli-Mya for the two species, 210 Mya between the
hood analyses of melecular data and constraints group of 7bdea and Leptqpter iasnd the rest ofthe
from a reassessment of the fossi rlecord, Pryer et aL familM and 150 Mya between the O. jmponica group
(2004 be)stimated that basalmost fern families and subgcnus Plenasium.
diverge dduring the Carbonifero uasnd Jurassi cA. Another divergenc etime estimate was made
most basal fern clade of Ophioglossaceae and fbr extant lycophyte sbased on rbcL sequences
Psilotacea eappeared near the end ofthe Devonian (Wikstr 6&m Kenrick 200l). By calibration using
(36 4Mya) and the two familie sdiverge din the several fbssi levidence constraints Wikstr6m &
Late Carboniferou wsh,ile tha tofMarattiaceae and Kenric k(200 1es)timated tha tthe divergen cteime of
Equisetacea aeppeared in the very Early Caifboni-the ligula theeterosporo ugsrou p(Isoet Seest,agi-
ferous (35 9Mya) and the familie sdiverge dshortly nella) and the nonligulate homosporous fycopodia-
after (35 4Mya). Osmundaceae, the basalmos tlep- ceae is 393 Mya, that oflsoetes and Setaginel lias
tosporangiate ferns, diverged in the middle 375 Mya, and tha tefHmperzia (al sPhoylloglossum)
Carbenifero u(s32 3Mya), Exceptional lHyym,eno- and a group of LIFcopodi uanmd lycopodie ilsla
phyllopsidaceae, a nontree-fern member of the 351 Mya. Data suggest that ,in sharp contrast, the
lower tree fern group, diverge dmuch late rin the diversificati oonf epiphytic species of Htipereia,
[[lertia Trwyo. aquatic fer nfamilie sA,zollacea aend likc polypodioid ferns, occurred in the Late
Salviniaceae ,diverge din the Cretaceous. Cretaceou ssubsequently to the diyersifica toifon
Among recent progres sin the systematics and anglosperms,
divergenc teime estimate ofparticular fern groups, Des Marais et al. (2003 p)erfbrmed a rnolecu-
most noteworthy is Yatabe et al.'s (199 9wo)rk on lar analysis of Equisetum. They found that subgen-
Osmundaceae, Traditionall yb,ascd on morpholog- era Himpochaet eand Equisetum are each mono-
ica ldata, Osmundaceae are classified into three phyletic ,except fbr E. bagotense whose placement
genera ,Osmunda, Leptopteri sand 7bctea ,among is arnbiguous. Divergenc etime estimation shows
whieh Osmunda are subdivided into subgenera that the modem Equisetu mbegan divergence in the
Osmundu, Osmundostrum and Plenasium (some-Early Cenozoic (Eoce n40e M;ya) and the two sub-
times raised to genera) ,By marked contrast to this, genera diverge din the Oligocen e(30 Mya), i,e.,
Yatabe et aVs (1999 r)bcL tree shows that O. cin- much late rthan the Paleozoic origin of Equiseta-
namomea is sister to all other members ofthe fam- ceae. The estimate is in accordance with fbssi elyj-
ily includin gO. ctaytoniana, although the two dence .A distin cgtap between the two divergence
species are usually assigned to subgenus Osmuncin- times indicat tehsa tcladogenesis seldom occurred or,
strum. Osmundaceae except fbr O, cinnamomea more likel ye,xtinction often happened during the
diverge into two clades. One comprises 7bdea and period.
Leptopter iasnd the other comprises O. claytoni- In conclusion, molecular divergenc teime esti-
ana and a subclade comprising a subgroup of O. mates have demonstrate da historica lstructure of
y'oponic aO,. Iancea and O. regalis and subgenus pteridophy tfebsr over 400 million years .Estimation
Plenasium. This phylogeny suggests titt mloerpho- will become more accurate, as fossi alnd melecular
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data will be added and calibration methods will be cheophytes (Kenri c20k00) .Kato & Akiyama (in
improved. press )interpre ttehdat the branche daxis of the poly-
sporangiophyte with a persiste anptical meristem is
Cladist iAcnalyses a novel vegetative organ interpolat eidnto the
bryophyticlife thebryophyte
cycle, and sporophyte
Pryer et aL (1995 u)ndertook the firs ctladistic is an archaic sporangium with the fbot ,The nonva-
analysis of phylegenetic relationships and mor- scular polysporangiat eplant shad hydroid-li ckoen-
phological evolution of ferns T,hey used 77 vege- ductin gcells without secondary walls, The vascular
tativ eand reproductive characters fbr 50 taxa rep- system increasing dleyvelop easd the axes enlarged.
resenting all major groups .Pryer et al. (1995)Early vascular plant shad three differe tnytpes oftra-
hypothesiz eand evolution ofsporophytic and game- cheids, S-typ e(e. gS.en,icauli osf Rhyniopsida),
tophytic characters, based on a phylogenet itcree G-type (e. gG.os,slingi aof Zesterophyllopsida),
constmcted from combined morphological and mol- and P-type (e. gP.s,ilopItyto nof Euphyllopsida)
ecular data .The characters examined includ veena- (Kenri c&k Crane 1997) .S-type tracheids have
tion, hydathodes ,dermal appendages, sporangial helica lwall thickenings comprising a thin decay-
annulus and stalk, exospore, gametophyte hairs, resistant inne rlaye r(faci tnheg primary cell wall)
antheridium position ,and the nurnber ofantheridi- and a spongy outer layer .G-type tracheid shave
um wall cells. annular thickenings comprising a decay-resistant
Rothwell (1999 i)nvestigate tdhe cladistic phy- inne rlayer and a nonresistant outer laye zP-type tia-
logeny ofpteridophytes using morpho]ogical char- cheids had scalarifbrm thickenings comprising a
a¢ters ofboth livin agnd fbss ipllants w,ith special decay-resist ainntne rlaye rand pit chambers, and a
reference to fems in a br.oad sense. Stauropteridnonresistant layer ,Fossil wsith G- and P-type tra-
fern s(foss ialres )a monophyletic group that is cheids are grouped in eutracheophytes, while
basa lin the pteridophy taensd siste rto the rest ofthe Rhyniopsida with simple S-typ etracheids is primi-
plants P.silotacea eis next basa land most closely tive tracheophytes placed outside the eutracheo-
related to extinct primitive vascular plants, phytes .Friedman & Cook (200 s0tr)essed the hypo-
Cladoxylalean fern splus Zygopteridalean ferns thetica levolution of development eallaboration
(bot ofhwhich are fossil fso)rm a clade tha tis more involvin tghickening of the decay-resist alnatyer,
closely related to equisetophytes and seed plants from S-typ eto G-type ,then to P-typ eand eventually
than to other group soffemlike plant s[,[he basa lfi1- seed-plant type with no decay-pron elayer.
icalea nfern sinclud elivin gbasal fern sand the Living eutracheophytes are divided into
Paleozo ifcern sthat are considered to be coenopterid tycophyt aindna Euphytlophytina. This biphyletic
ferns D,ifferenc ebsetwee nRothwell' (s199 9an)d classification is in agreernent with two branching
molecular phylogenie smerit furthe ranalyses, pattern osfroots in pteridophytes ,i.e .,apical and
becaus ethe former deal twith both 1ivin gand extinct dichotomou sbranchin gwith exogenous origin in
plants ,while the latt edreal twnh ljvin pglant aslone. lycophyte asnd subapical or monopodiai one with
Kenrick & Crane (1997 )canied out a large- endogenous origin in fern s+ Equisetum (Kat &o
scale cladistic analysis efearly 1and plant evolution, Imaichi 1997). Zosterophyllopsid aofLycophytina
based on evidence from both foss ialnd extant plants.has enations on axes and Lycopsida has micro-
According to them, polysporangia tperetracheo- phyllous leayes w,hich are derive dfrom enations.
phyte swith multiple sporangia on branched axes Leafy Euphyllophyti nhaas euphyllous leaves and
(e. gA.g,laopbyton, Hbrneqp]tyton) preceded tra- ancestral fossi lhsad leafle sbsranch systems or
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A9d
Heterospory
@
o
o 9)g
o 9dU
Homospory
o
Sporc - Dispcrsa l - Fertilization
Fic ]2.. Hypothetica slpore disper saandl subsequcnt fertiliz aitn ihoentcrospor potucsridophyte cso,mpared with those ofhomesporous
pteridophyte sI.n homesporous plants cither intragaJnetophy tsiclcfing or intcrgametophyt icrcossing occurs in bisexua lgame-
tophytes deriyed from separately disperse dspores. Gametophytes are exosporic. In heterosporeu pslant sco-dispersal ofmegas-
pores and microspares rnay occur by sarne migrating vector oT spore pollination ,and intergametoph yctroisscing occurs
between connected or nearby unisexual gametophytes ,Garnetophyte sare endosporic.
primitive leaves .Euphylls are considered to have vascular plan tgroups durin gthe Middle Devonian
been derived from telomes, i.e .a,ncestral branched and Permian (Batem a&n DiMichele 1994, Bateman
axes, but to have appearcd independent liyn differ- 1996) ,They are Lycopsid a(Selagine l[leaxlteasnt
ent lineage s(a tleas tferns p,rogymnosperms, and Selaginella ]and Rhizomorphales [Isoetes]),
Beerling (2001) Osborne Zosterophyllopsi(dBaarinophytaSplheesn)op,sida
equisetophytes), et al, and
et aZ. (200 4su)ggested that changes of the Devonian (som eSphenophyllales), Pteropsida (Stauro-
atmospheric environment (C0 2concentration, tem- pterida]es )an,d Progymnospermopsida (some
perature )and the histologi csatlructure of leaves Aneurophyta]es, some Archaeopteridales,
(stoma dteansit ys,urface area, conducting system) Protopityale sC,ecropsidale sa,nd some Noeg-
force dthe long (40 million years )dela yof evolution gerathiales )I,n comparison, a few heterosporous
ofmegaphylls behind leafle saxses or microphylls. fern sor Pteropsid a(Salvinia c[eSaZezlvi Anzioall,a],
Marsileaceae[imrsilPeialu,lania,Ragnellidium],

Heterosporous Pteridophytes PlaCyzoma )evolyed more recently, probably in the
Jurassic later(Pryer 2004b).Thus,het-
or et al.
Heterospor yis considered to be an evolutionary erospory appeared iterativ etlhyroughout the his-
prerequisi ttQe a secd habit .A group of hetero- tory ofpteridophytes. Heterospory did not evolve in
sporous progymnosperms evolved int oseed plants, early vascular plant ssuch as Cooksoniopsida,
which have thrived in the Mesozoic and Cenozoic, Rhyniopsid aT,rimerophytops ainad Cladoxylopsida
most remarkably as angiosperms in the Tertiar yup that lived fi'om the Late Siluria nto the Early
to the present .This clade ofprogymnosperms and Carboniferous.
seed plants is coined lignophytes characterized by Heterospory is Iinked to gametophyt eunisex-
the secondary vascular tissue ,Heterospory appeared uality: megapores exclusively produce female
at minimum 10 times in most (5 )ofmajor lower megagametophytes and microspores produce rnale
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microgametophytes (Fi g2.). It results in obligate archegonia. After one or several cell diyisio ntshe
intergametophyt iouctcrossing, which maintains microspore becomes a prothallia lcell and (an)
geneti vcariations that provid esource ofevolution to antheridium initial( asn)d, subsequently it (they)
be selected. In this aspect, heterosper yis mere develop( si)nt oantheridia, which are embedded or
advantageous than homospory that allows intraga- protmded (Smit 1h955) .The rnegaspore undergoes
metophytic selfing, although i tis more disadvanta- cell division sin the dista lpart and free nuclear
geous in that disperse dspores, if single, cannot divisio nisn the rest, and archegonia are formed in
FIIius,
lead to fertiliza tanidon colonization in a new loca- the cellular dist at1issu e. the male gametophyte
tion except for apogamy Platyzom ashows incipientis mostly antheridial, while the female gameto-
heterospory (Tryo 1n964). The megaspore is two phyte has foed reserves that are alse provided to the
times large rthan the microspore, a small size difi embryo. Sexual organ differentiati oocncurs at the
ferenc ecompared to about 1O times 1arge rmegas- initi astlage of gametephyte development a,nd the
pores of genuin eheterosporous pteridophyt eTshe, female garnetophy tberidge sthe sporogenesis and
developsinto fi1-
microspore germinates and a small embryogenesis.
amentous (exospor imacle) ,gametophyte, while In heterosporo pulsant ssexual determinati iosn
the megaspore develops into a 1arge spatulate female sporophytic and, unlike that ofhomosporous plants,
gametophyte ,which forms lobe swith antheridia, is not infiuenc ebdy the environment. DiMichele
eyentually becoming hermaphrodit i(cDucke t&t et at, (198 9a)nd Bateman & DiMichele (1994)
Pang I 984) .Subculture pdortion osfthose gameto- argued that the precociousne sfsor endospory and
phytes originating from either spores yield male, gametophyt esexual maturation may possibl ybe a
female and hermaphrodit giacmetephyte ast various result ofa kind of heterochrony (i. ep.ro,genesis).
proportion Rse.sults indica tteha tthe species has an Earlie ridea sof gradual evolution (e. gT.i,ffhey
association between gametophyt emorphogenesis 1981) claim that heterospor wyith exosporic uni-
and sex organ formatio nb,ut the association is not sexual gametophytes, as seen in Platyzoma ,is an
absolute. In Ceratopter tihsalictroid e(sSchedlbaueevrolutionary intermedia bteetween homospory (and
1976) and other homosporous fems, large rspores exospory) and heterospory with endosporic game-
from a unimodal spore-size range tend to develep tophytes. Even though endospory fbllowed het-
into bisexua lgametophyte sand 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 c)ompared the spore. DiMichele et al. (198 9an)d Bateman &
sexual behavior of gametophyte sofhQmosporous DiMichele (199 4d)o not support this gradua levo-
ferns with mixed and allopatric er allochronic lutio nhypothesis because of the disadvanta gtehat
gametangia a,nd suggested that such association of free-livi n(gexospo runiisce)xual gametophyte csan-
gametophyte dioecis mand dimorphism evolution- not control the sex ratio and lose sexual flexibility
arily may have preceded true heterospor ayn,d sex (e,g ,la,cking of intragametophyti cselfing).
determinati omany have been accelerated from the DiMichele et aL (198 9an)d Bateman & DiMichele
gametophyt estage to sporogenesis, (1994 i)nsis tthat heterospor yis not a necessary
Endospory is exclusively associated with het- antecedent to endospory, but rather may have
erospory in livin gpteridophytes (Fi g2,), In evolved as an epigenetic consequence of endospory,
endosporic species the gametophyt edevelo pwhsile They hypothesiz etdha tgametophyt iuncisexuality is
a most portio nis enclosed within the spore wall a positio neffect of the metabolic microenviron-
fordeveloping female
and precociously produces either antheridia or ment spores: megaspores with
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