Molecular and Fossil Evidence on the Origin of Angiosperms

29 Pages·2012·0.81 MB·English

by  James A. Doyle

EA40CH13-Doyle ARI 23March2012 14:10
Molecular and Fossil Evidence
on the Origin of Angiosperms
y.
nl James A. Doyle
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viewonal Demepaialr:[email protected],UniversityofCalifornia,Davis,California95616;
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Earth Planet. Se University - oT1C0noh.lp1iisn1year4ri6agtt/ihcaetlnea(cid:2)n’rcstuhdr2.eoa0vin1:-n2euabraytlhrAe-v0ni4ne2wu7as1l.o1Rr-eg1v0i5e3w1s3. AMthbeoislretcrinuaclcartreadsaintagomnorreplahtoiolongsihciaplsdwiviethrsinityanthgrioosupgehrmthsecoCnrfietramcetohuesvrieeflwecttheadt
ev. Stat Allrightsreserved their evolutionary radiation. Despite the early appearance of aquatics and
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y veinedleaves,multipartedflowers,uniovulateascidiatecarpels,andcolumel-
b
larmonosulcatepollen.Moleculardataappeartorefutethehypothesisbased
onmorphologythatangiospermsandGnetalesareclosestlivingrelatives.
Morphologicalanalysesoflivingandfossilseedplantsthatassumemolec-
ularrelationshipsidentifyglossopterids,Bennettitales,andCaytoniaasan-
giospermrelatives;theseresultsareconsistentwithproposedhomologiesbe-
tweenthecupuleofglossopteridsandCaytoniaandtheangiospermbitegmic
ovule.Jurassicmoleculardatesfortheangiospermsmaybereconciledwith
thefossilrecordifthefirstangiospermswererestrictedtowetforestunder-
storyhabitatsanddidnotradiateuntiltheCretaceous.
301
EA40CH13-Doyle ARI 23March2012 14:10
INTRODUCTION
Inthepast20years,phylogeneticanalysesofDNAsequencedatahaverevolutionizedthinking
abouttheoriginandevolutionofmanygroupsoforganisms.Theimpactofmoleculardatahas
beenespeciallyprofoundinangiosperms,orfloweringplants,whichrosetodominanceinmost
terrestrialecosystemsduringtheCretaceous.Bythelate1990s,analysesofmultiplegenesledthe
AngiospermPhylogenyGroup(1998)toproposeanewhigher-levelphylogeneticclassificationof
angiosperms,whichhasremainedremarkablystablewithstudiesofincreasingnumbersofgenes
(Angiosperm Phylogeny Group 2009), including nearly complete chloroplast genomes (Jansen
etal.2007,Mooreetal.2007).Asinothertaxa,molecularphylogeneticstudiesofangiosperms
haverevealedbothagreementswithpreviousideasderivedfromthefossilrecord,whichcould
betakenasreaffirmingthevalueofbothfossilandmoleculardata,andapparentconflicts,which
y.
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s.oruse Thisreviewexploresareasofcongruenceandconflictandwaysinwhichconflictsmightbe
annualreviewFor personal rtloeiefomsanonalwvgroeyiodudsl(ipdcvefeir.nrmDvsiosfiol,cyvoaelertpiso2ry0ninm0,a1eapm)ro.ilImpyhfoaoanrcspuiuzhsniinoedgnse,ratbshptyeahntoyrdarloiinnggsgiefnonoroefmfttihaacnetfigrooairnomigsopeifnwesrootmrfruktsch,.taeAusdrsdeiusisstciktcninencsogtsiwufvuineslhnisneoedwlrueftirlniaoottmnreidnttoshpieltcahifnreeteaspvt,ruoaorlnubed--s
ww.12. secondarilyanunderstandingofextrinsicaspects,suchaswhenandwherethesechangesoccurred
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26. of L unusuallymysterious,becauseofboththelackoffossiltaxaintermediatebetweenangiosperms
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ci. 2012.4Scientific ba2p0epe0ne9a)i,rdetehdna“ttisfiutheddedeognrrlocyuo”pminop“ramirgeoidndawetrietndhfoadnrivmde”rdslieevdemrtsooidfiseuerdgngbteeasxftoiaor.enTsth,hgeeoriCensrguelbttaainccegkotiumosDpirnaersswsoiimonneintah1ra8eta7a9wn(giFtihoriseapdepmromaonrs
Earth Planet. Se University - faoonfsgdsTiieolphsroipesseciprotmiirocdtsn.uoriTrneihgtbehienebgaeCatesnrtdetditonaecvcteerhoolaoupnpsigceaeadslwtauhiprteelhoasnrusydtlutswdoiainfesistnthhocerafePtfaoeosrsifmnsiAglixlapyenolerolqloreudnTa,(br1wli9eahs5csi2lciic,hm1apan9tr7deo0siv.)ni,dvwaeddheoedvplioodwsetnluaclnaedteobdnatsflhinoa-st
ev. Stat ras in geographic areas where plant megafossils were unknown and broader representation of
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y transportedfromtheuplandsifangiospermsweregrowingthere,andfoundthatEarlyCretaceous
b
angiospermpollenwasmuchlessdiversethanexpectedfromfossilleafidentifications(Scottetal.
1960,Brenner1963).Mostsignificantly,thesequenceofappearanceofmajorangiospermpollen
typesagreedwithhypothesesonpollenevolutionderivedfromcomparativemorphologyofRecent
plants(Figure 1)(Doyle1969,1978;Muller1970).Thefirstangiospermpollenwasmonosul-
cate;thatis,ithadasinglefurrowforpollentubegermination,asingymnosperms,monocots,
and “magnoliid dicots,” which were thought to include the most primitive angiosperms. This
pollen was identified as angiospermous by its columellar exine structure, with radial rods con-
necting the inner and outer wall layers (nexine and tectum, respectively). Such pollen is now
known back to the Hauterivian or Valanginian (Trevisan 1988, Hughes 1994, Brenner 1996).
Monosulcates were followed by tricolpate pollen, characterized by three longitudinal furrows,
302 Doyle
EA40CH13-Doyle ARI 23March2012 14:10
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ev. Earth Planet. SState University - utpGeytsepouaaenarl.eldfl1doyw9riai7ntnn7hat;eth)hS,evecabhlsauArtttalembntBihkaajaen1orr9rreaie8,ttmy3tno;oioaPofrn,e“tnhdtohneirceryAony1tpsm9wt,8”ieia6drnn;edoRolwpeferSgkleaanoctleuoiitdtwu&hedndAeVtsbmoiay(feSnormoariucm1oat9nh,a8oeA9crsf;lnuraDildccLeoaaa,tynuealasernmad1(sB9ietard9h)e2.een;TuMnIdbheiirricdsaod1hit9lsisem7.tE6Th2,ear0s1ibct09oa2(9Nsl;6piSc;oactrpDhetohsrolaealynerplnnke-
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by joinedintheCenomanian(LateCretaceous)bytriporatepollenoftheNormapollesgroup,with
three round apertures, as in wind-pollinated Fagales, which most botanists regarded as highly
derived.
Theseobservationsledtoaconsensusthatthemainradiationofangiospermsoccurredduring
theCretaceous.Severalauthorsnotedthatangiospermsmighthaveexistedearlier,but,ifso,they
musthavebeenlowindiversityandadvancementtohaveescapeddetection(e.g.,Doyle1969,
Muller1970).Thecongruenceofthestratigraphicsequenceofpollentypesandtheirpresumed
evolutionary sequence would make no sense if angiosperms had already diversified in a hidden
homelandarea;thereisnoreasontoexpectthatgroupswouldmigrateintobetter-knownareasin
theorderinwhichtheyhadevolvedmuchearlier.Axelrod(1970)suggestedthatpollenevolution
mighthavelaggedbehindthesystematicdiversificationofangiosperms,butothersarguedthat
www.annualreviews.org • OriginofAngiosperms 303
EA40CH13-Doyle ARI 23March2012 14:10
this was inconsistent with the systematic congruence of pollen and classification (Muller 1970,
Walker&Doyle1975).
ThispicturewasconfirmedbystudiesonCretaceousangiospermleaves,whichhadbeenne-
glectedsincetheearly1900s.Leavesweretraditionallythoughttohavelowsystematicvalue,but
thisviewwaschangingwithmorerigorousmethodsofanalysisofleafcharactersandsurveysof
theirsystematicdistribution(Dilcher1974,Hickey&Wolfe1975,Doyle2007).Studiesofan-
giospermleavesinthePotomacGroupoftheeasternUnitedStates(Figure1)showedapattern
of morphological diversification through time comparable with that seen in the pollen record
(Doyle&Hickey1976,Hickey&Doyle1977),bearinginmindthatthesectionbeginslateinthe
monosulcatephase.InthelowerPotomac(ZoneIofBrenner1963),probablyAptiantoearliest
Albian (Hochuli et al. 2006), angiosperm leaves are rare, simple, and usually pinnately veined,
y. with unusually irregular venation. Similar features occur in Recent “woody magnoliid” groups
nl
go withmonosulcatepollen.Afewarepalmatelyveined,asin“herbaceousmagnoliids.”Ternately
s.oruse dissectedleaves(withthreefolddivisionoftheblade),asintheeudicotorderRanunculales,appear
viewonal alongwiththefirstraretricolpatepollen(Vitiphyllum).Moreabundantanddivergentleaftypes
annualreFor pers abplepewairthinlivthinegutpripceorlpPaotetogmroaucp(sZ,osnucehIIa,smpeidltdalteealenadvelast(eNAellubmiabni)t,esm)sainmyiloarf twohtihcheaaqreuactoicmgpeanrua-s
w.2. Nelumbo(lotus),palmatelylobed“platanoids”comparedwithPlatanus(sycamore),andpinnately
w1
w1/ dissected and compound leaves (Sapindopsis) now also known to be related to Platanus (Crane
om 05/2 etal.1993).MostoftheseleaveshavemoreregularvenationthanthoseinthelowerPotomac.
d fron Consistent sequences are known in western North America, Portugal, Kazakhstan, Colombia,
Downloadeomonosov B20ra0Tz9i)hl.,easnedadAvragnecnetsindaid(Dnooytlhea&veHaigcrkeeayt1im97p6a,cPtoonnsd1i9sc8u4s,sMionoshrof&thFerioisri2g0in00o,fAarncghiaonspgeerlsmkys;etthaely.
26. of L providedmoreindicationsoncharacterpolarityandtimingoftheradiationthanonrelationships
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ci. 2012.4Scientific msJeuoerdansofsesicru)nl,csaasntuedcphpooalsslseginblol(eDsshooopymtleeor1liod9gs7i(8ea)sc.toMufaotlhlsyetPdoieusrtcmeursisaininot)ne,gscuoomrfyteshnteotsooprfeitrghmiensbc(ieTtnertgieamrsesidcica)o,nnagnsioods-CpcaealrylmteodnoiMavu(emlseoawzinoitlihyc
Earth Planet. Se University - tDohluielBtcishoeeegneridinz1-enb9die8nab1gry)i.inndgitshccouevp1eu9rl8iee0soso,ffuthfnoedsseserilsttflaaxonawd(ienGrgsaauonsfdstehfnreu1Cit9sr4e(6tFa,rcSieitsoe1ub9sb8ian4ns;gFi1or9si7ips4ee,rtmDalor.ey2cl0eo0r10d9,w7280a,s0R6fuaer,tt2ahl0lea1rc0rkae,v&b-,
ev. Stat 2011),mostlyinthemesofossil(millimeter)sizerange.Contrarytoearlierassumptions,flowers
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Annu. Mosco aarnedostfutedniewdewllitphrsecsaenrvneindgaeslelicgtnroitnemoriccrhoascrocopayloarnXd-craanymbeiceroxttroamctoegdrafrpohmy(sFerdiiismeetnatls.2b0y09si,eFvirniigs
y & Pedersen 2011). Flowers have been the mainstay of angiosperm systematics since Linnaeus,
b
largelybecausetheyaresorichincharacters.Furthermore,fossilflowersoftenhavepolleninthe
stamensoronthestigma,whichallowsintegrationwiththedispersedpollenrecord,andtheycan
sometimesbeassociatedwithleavesandwood.Studiesoffossilflowershavebroadlyconfirmed
thepicturebasedonpollenandleaves,buttheyprovidemoredetailontheactualcladespresent.
However,palynologyremainsvaluablebecauseofitsgeographicandstratigraphiccoverage,which
increasesconfidenceininferredevolutionarypatterns.
These advances were paralleled by the expansion of cladistic (parsimony) methods for phy-
logenyreconstruction,initiallyusingmorphologicaldata.Althoughsomemorphologicalcladistic
resultshavebeenrefutedbymolecularanalyses,othersthatwerecontroversialatfirsthavebeen
confirmed.Inaddition,thecladisticapproachgreatlyclarifiedevolutionaryquestionsbyforcing
304 Doyle
EA40CH13-Doyle ARI 23March2012 14:10
Extant sister group Crown group
Stem relatives
Crown node
Stem lineage
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w.2. systematists to formulate more explicit hypotheses on phylogeny and its relation to character
w1
w1/ evolution,whichisnolessimportantinthepresentmolecularera.
om 05/2 Molecular results concern only crown groups (a crown group consists of the most recent
d fron commonancestorofalivingcladeandallitsderivatives),andnotthestemlineagesconnecting
ownloademonosov c(Droowynleg&rouDposnwoigthhuoene1a9n9o3t)h.eFrr,oomreaxtpinhcytlborgaenncehtiecsp(soteinmtroeflavtiievwes,)tfhreomortihgeinseolfinaenaggieoss(pFeirgmusreca2n)
Do be broken into two related problems, which are loosely comparable with the classic questions,
26. of L “Whatwerethefirstangiospermslike?”and“Whatdidtheycomefrom?”Thefirstproblemis
301-3brary wherethecrowngrouptreeisrooted,orwhichextantlinesaremostbasal(attachedtothemost
0:Li basalnodes).Basaldoesnotnecessarilymeanprimitive:Livingrepresentativesofbasallinesare
ci. 2012.4Scientific uHpsaourswailmelyvoemnr,yogr(eiovroernreleltahstseesdcphcearcriitaaelcritzieaer)dstrooefloalpitvitviimnegtizoteatxhcaheaalronandcgtte-hdreesattadrteecesotmoonmpotohlnoegatyrn,ecewesaetnocdran(eCsutrisimsepatth&eetChpoerionakncic2pe0lse0tr5oa)fl.
Rev. Earth Planet. Sw State University - seatmhtxcaaealtymaecd,blpoeeels,veemei,tsnitoifsoirtneumhttoeoghrrrseeltoeaaupsbrpsaesrsedtsnoewimrcfoietvohooenerdfiao,mdnbuaogutsarittoeofisrflporisneemeecrvmoseonwrusastiatltgrrhorueuotc(htuttgheptrehsosian(usamepstatseoraaepstrets-eatdatbkoesenwabionnnrwacganentpsch,pthierrtiaonslmia.gscTatiheynhr;beBagersasoepetecuromiopsens)sai.dbnbAlpeeeglrtaotoaiownbl.r,ltee2ohmc0ueo0tnbig6ssur)tw.olrkFuhuopocarsttf
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by ofcircularreasoning:Wheretheingrouptreeisrootedmaydependonwhichtaxaareconsidered
theclosestoutgroups,andviceversa.Thisproblemisbestresolvedbysimultaneousanalysisof
bothingroupandoutgrouptaxa.
Most morphological cladistic analyses of seed plants indicated that angiosperms were most
closely related to living Gnetales and Mesozoic Bennettitales and Pentoxylon—the anthophyte
hypothesis,sonamedbecauseallthesetaxahaveflower-likereproductivestructures.Thisrecalled
viewsofArber&Parkin(1907),whoalsoassociatedangiospermswithBennettitalesandGnetales.
However, some analyses linked anthophytes with Mesozoic seed ferns (Crane 1985, Doyle &
Donoghue 1986), others associated them with coniferophytes (Nixon et al. 1994, Rothwell &
Serbet1994),andsomemovedCaytoniauptoapositionsistertotheangiosperms(Doyle1996,
2006,2008;Hilton&Bateman2006).Rootingsoftheangiospermswerealsoinconsistent;the
www.annualreviews.org • OriginofAngiosperms 305
EA40CH13-Doyle ARI 23March2012 14:10
basal lines in some analyses had multiparted flowers (Magnoliales: Donoghue & Doyle 1989;
Calycanthaceae:Loconte&Stevenson1991;Nymphaeales:Doyle1996),whereasthoseinother
analyseshadsimpleflowers(Chloranthaceaeand/orPiperales:Nixonetal.1994,Taylor&Hickey
1996).
Molecularstudiesprovidenodirectevidenceonrelationshipsofangiospermswithfossils,but
theyalmostuniformlyrejectthemainconclusionabouttheirrelationshipswithlivingtaxathat
morphologicalanalysesagreedon,namelytheirconnectionwithGnetales.However,molecular
datahaveessentiallyresolvedtherootingproblemandtherebygreatlyclarifiedthemorphology
ofthefirstangiosperms.Thenextsectionsexplorethestatusofthesephylogeneticquestionsin
light of molecular and fossil data and discuss the problem of the time and environment of the
origin of angiosperms. Although the topic is the origin of angiosperms, I devote much space
y. to the Cretaceous radiation because its interpretation is essential for reconstructing ancestral
nl
go statesandgainingperspectiveonconflictsbetweenmolecularandfossilevidenceontheageof
s.oruse angiosperms.
viewonal
annualreFor pers MOLECULARANDFOSSILEVIDENCEONTHEFIRSTANGIOSPERMS
w.2. Thefirstmolecularanalysesofangiosperms,basedonsinglegenes,gaveinconsistentrootings.
w1
w1/ RibosomalRNAidentifiedNymphaeales(waterlilies)asthesistergroupofallotherangiosperms
om 05/2 (Hamby & Zimmer 1992), whereas the chloroplast gene rbcL placed the rootless aquatic Cer-
d fron atophyllum in this position (Chase et al. 1993). However, since 1999, multigene analyses have
Downloadeomonosov y1ari9ee9lld9ae,rdPgearlreykmiinnassroeknnasbeitltyivaelc.ot1on9sc9ihs9to,eiQncetiuoafneotduastl.gta1rto9isu9tp9ics,aP(lGl.ySr.awSheoalmllt-iss&ueptIplaeolsr.t21e09d0999r)e,.sDTul.htEse.s(SeMoalnattiashlyeeswteassl.(&s2e0eD0F5oi)gn,uowgrhehicu3he)
26. of L placedthreelinescontaining∼175speciesatthebaseofthetree,intheso-calledANITAgrade:
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ci. 2012.4Scientific afifonvrgeiAcolmsapdbeeorrsme:lClasph,elNocriyeamsntfphoharamceeaaaleec,so,nroIeltleigcdrioafluoeprs,tnhTaemriirmesdeimnmipae,lseaanflndogwioAesurpsset;rrCombeasria(lteCoypaahn.)ytliTlnuohmee;trMeamla.ga2ni0no0iln7iig)d,am>e,9aid9ne.9au%npeoowff
Earth Planet. Se University - mapgnrooadlldnePeonpi.wphWeiytrhlaietltmehiscion(ssietenlnuycsdluetirc,diocicntoosgln,psRAaistraetinisnputogonllcooluecfnlhaMilbaeacesgel(oanpweoo)l;piaapmlvieeaosssn,t,oLbccouaourtttersea;rclacelanusd,dpeCse)taueandrnemidclloeasdtecsev,Paeweerani(tltihanopcttherluitecadroliallniepng,aetmWseofaoisnntrtdmoerfdaaewcrbehiaavisecea)hdl,
ev. Stat havepentamerousflowerswithaperianthdifferentiatedintofivesepalsandfivepetals,aswellas
Rw
Annu. Mosco tricSoolpmoeramteopleoclulelnar.resultsthatcontradictedolderviewswereanticipatedbymorphologicalanal-
y yses, such as the monophyly of eudicots and the association of Aristolochiaceae with Piperales
b
(Dahlgren&Bremer1985,Donoghue&Doyle1989).However,morphologicalstudiesgrouped
Piperales,Nymphaeales,andmonocotsineitheraparaphyleticgrade(Dahlgren&Bremer1985)
oraclade(Donoghue&Doyle1989),ratherthanplacingNymphaealesintheANITAgradeand
Piperales in the magnoliid clade. In these cases, morphology was overruled when morphologi-
calcharacterswerecombinedwithsequencesofthreegenes(Doyle&Endress2000).Persisting
areasofuncertaintyconcernwhetherAmborellaandNymphaealesformtwosuccessivelinesora
cladeandthearrangementofthefivemesangiospermclades.InthecombinedanalysisofDoyle
&Endress(2000),carpelfeaturesretainedfromtheANITAgradeoverruledmoleculardatain
placingChloranthaceaeatthebaseofmesangiosperms(Figure3).Doyle&Endress(2000)did
not include Ceratophyllum, but morphological data of Endress & Doyle (2009) linked it with
306 Doyle
EA40CH13-Doyle ARI 23March2012 14:10
Mesangiosperms
Magnoliidae
Austrobaileyales Piperales Magnoliales
Nymphaeales Chloranthaceae Canellales Laurales Monocots Eudicots
AmborellaHydatellaceaeArchaefructusCabombaBraseniaNupharMonetianthusBarclayaNymphaeoideaeAustrobaileyaTrimeniaAnacostiaSchisandraceaeIlliciumCeratophyllumHedyosmumplantAsteropollis AscarinaSarcandraChloranthusplantPennipollis CanrightiaPiperaceaeSaururaceaeLactorisAsaroideaeAristolochioideaeWinteraceaeWalkeripollisCanellaceaeMyristicaceaeMagnolioideaeLiriodendronArchaeanthusEndressiniaGalbulimimaDegeneriaEupomatiaAnnonaceaeCalycanthoideaeIdiospermumVirginianthusAtherospermataceaeGomortegaSiparunaceaeHortoniaMollinedioideaeMonimioideaeMauldiniaLauraceaeHernandioideaeGyrocarpoideaeAcorusLiliaciditesAraceaeTofieldiaceaeButomusAponogetonScheuchzeriaMelanthiaceaeNartheciaceaeDioscoreaceaeEupteleaPapaveraceaeCircaeasterLardizabalaceaeMenispermaceaeBerberidaceaeHydrastisGlaucidiumCore Ranunculaceae NelumboNelumbitesPlatanusWest Bros platanoidSapindopsisProteaceaeTrochodendronTetracentronSpanomeraBuxaceae
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Do
301-326. brary of L Carpel formATrsicmideinaitae p caaprpuealn oaf StratLiagtrea Aplhbyian – early Cenomanian
ci. 2012.40:Scientific Li EAIPnqlsitccueaiirdvtmieoaectdealiate L(E(iBaanutrcelalyu rB c–dao imrnsr,gei Pdm Tudoidlaerdnr Ael e–slbd AVioaepcndtkira, aenst?)c .)
ev. Earth Planet. SState University - FPfDfooihorsgysmyuilllo.retgePa&exr3noaEebptnailcbadclrteeerdespseoa(ots2ifmt0ib1ooa0nss)tsa,lpoaaanfnrdosgtiFimhoresoirpinsmei&roomunPsorepecdoloaesttrisitsoieaonnnnsdh(s2iebp0uas1ds1feirc)do.omCotsnoEalaronnerdasilrnyoedsfseisbcs&aroatefnDdDc.hooCeyysloelielno(2edrt0sic0abal9e.t)eh(,2itbn0had0es8enm)da,omoEsnetnsdpmoraoerfsslfesiomc&susolinaDlsriooianuyndsldeicc(moa2ut0oer0rssp9ethr)o,aoftFlioegrvgirioaiscpleauhtltiidacolan.pt(aoo2,sf0iwt0ciiao9trh)np,sel
Rw
Annu. Mosco pofrolovcidaelidtiebsywPh.Ker.eEtnadxareoscsc.urorhavebeendescribedinmostdetail.DrawingofalongitudinalsectionofanascidiatecarpelofTrimenia
y
b
Chloranthaceae.Inanalysesofnearlycompletechloroplastgenomes(Jansenetal.2007,Moore
etal.2007),AmborellaandNymphaealesformedtwosuccessivelines,Chloranthaceaewerelinked
withmagnoliids,andCeratophyllumwaslinkedwitheudicots,butastudyofmitochondrialgenes
(Qiuetal.2010)linkedAmborellawithNymphaealesandCeratophyllumwithChloranthaceae.It
isnotclearwhethertheseconflictsreflectbiasinoneortheothermoleculardatasetordifferent
evolutionaryhistoriesofchloroplastsandmitochondria,owingtoancienthybridizationorlineage
sorting(polymorphisminthecommonancestorandlossofdifferentcopiesinitsdescendants).
However,an analysis ofslowlyevolving chloroplastgenes (Moore etal.2011), which wereex-
pectedtobemorereliable,foundtheCeratophyllum-Chloranthaceaelink,whichmightindicate
biasesinthewholechloroplastgenomedatasets.
www.annualreviews.org • OriginofAngiosperms 307
EA40CH13-Doyle ARI 23March2012 14:10
These results provide an independent framework for the study of character evolution that
helps overcome the problems of circularity and outgroup choice that plagued morphological
analyses(Doyle&Endress2000,Zanisetal.2003,Endress&Doyle2009).Byplacingthreelow-
diversitylinesbelowthebulkofangiosperms,theANITArootingpresentsanear-idealsituation
forreconstructionofancestralstates.Usingparsimony,theancestralstateforsomecharactersis
ambiguousowingtovariationamongtheANITAlines,suchaswhetherfloralpartswerearranged
inaspiralorinwhorlsofthree,butmanyotherancestralstatesareclear.Thus,wecaninferthat
themostrecentcommonancestorofangiospermshadvessellesswood,pinnatelyveinedsimple
leaves(Doyle2007),monosulcatepollenwithcolumellarexinestructure(Doyle2005,2009),more
thantwowhorlsorseriesofundifferentiatedperianthparts(tepals),numerousstamens,andmore
thanoneascidiatecarpelcontainingasinglependentbitegmicovule(Figure3;termsdiscussed
y. below)(Endress&Doyle2009).ThetwoarrangementsofAmborellaandNymphaealeshavelittle
nl
go impactontheseinferences.
s.oruse TherelationoftheseresultstotheCretaceousrecordcanbeevaluatedbyoptimizingindividual
viewonal charactersoffossilsonamoleculartreeorbyanalyzingadatasetthatincludesbothfossiland
annualreFor pers lwivitinhgatdaaxtaa.sTethoefimdeoarlpahpoplroogaicchalmchigahratcbteerasftoortabloetvhidlievnincegaannadlyfosisssi(lHtaexramasnednm&oHleceunldarricchksar2a0c0te8r)s,
w.2. for living taxa, but so far moststudies have used a molecular scaffold approach (Springer et al.
w1
w1/ 2001),inwhichamorphologicaldatasetforlivingandfossiltaxaisanalyzedwiththearrangement
om 05/2 oflivingtaxafixedtoabackbonetreebasedonmoleculardata(Eklundetal.2004,Doyleetal.
d fron 2008,Friisetal.2009,Doyle&Endress2010,Friis&Pedersen2011).Thisseemsjustifiedon
Downloadeomonosov trbhouebtugthsrteoesuennoadsussguthhmatpthtafiootsntshsilesshahodaudvliedtirobenelatoteifvstefeolydssfiinelswtwhceohufaulrdtaucprtreeo.rbsaabnldytnhoattamffoecsttmthoeletocpuolalrogreylaotfiolinvsihnigpstaaxrae,
26. of L Molecular results confirm that the stratigraphic order of appearance of angiosperm pollen
0:301-3Library tayppeerstucroerrsetastpeonisdsmtoonothsueilrcasteeq,uaesnicne tohfeevooldluetsitonrec(Dogonyilzeab2l0e0a5n,g2i0o0sp9e).rmThpeolilnefne.rrPerdioarnctoesttrhael
ci. 2012.4Scientific ActietNsatlIreTaslA.aFnrdoosomsitliingpgho,tllaethnceowrneitftiohnrutehoheusasevtefeeceatxtuuimsrteesadnwldoonuggrldanbbueefloadrriefefixtchiuneletCtsotrreudtciastctueinroeguuswisewhrietfhrwooiumdteplbyoeliclnoegnnsroiedfceBorgeenndnizaeentd--
Earth Planet. Se University - (tosMhuuegsug,alaelnesrctreset1stit9chru7aal0tla,VteeDxaitloneayecnltgeusitmnertuiaacanrtluo.rrs1eee9ti7awct5uat,lshaWteceona-lcloukodmeleuremc&lolaenrlWln,aearacnlmtkdienoragnl1toAh9su8ous4ultc)gra.ohtHbestaohimlweeeyatvyaeelcenrts,uoammtnbodewlemaacssueslfoaaarrnriggtfririnoeoeasmplsleyitmrhmceposlno.ytrTitinghhuiain-st
ev. Stat of angiosperms as thought. The continuous-tectate stage may be represented by Hauterivian
Rw
Annu. Mosco p20o0ll1e)n.withaverrucatetectumreminiscentofAmborella(Hughes1994;Doyle2001,2005;Hesse
y Molecular trees imply that tricolpate pollen, the next major fossil type, evolved once from
b
monosulcateonthelinetoeudicots.Tricolporatepollenwasderivedfromtricolpateseveraltimes,
asinferredfromthevariedsculptureoflateAlbiantricolporates(Doyle1969,Furnessetal.2007).
Mostbasaleudicotsaretricolpate,butafewshowisolatedoriginsoftricolporatepollen(some
Menispermaceae,Sabiaceae,Buxaceae).AmongPentapetalae,tricolpatepollenisretainedinmany
SaxifragalesandCaryophyllales,butRosidaeandAsteridaearebasicallytricolporate.Triporate
pollenwithgranularexinestructure,asinCenomanianNormapolles,evolvedfromtricolporate
withinwind-pollinatedFagales(e.g.,Betulaceae,Juglandaceae)andinthewind-pollinatedsub-
groupofRosalesthatwasformerlycalledUrticales(Doyle2009).
SimilarcongruencecanbeseenwhencharactersofCretaceousleavesareplottedonmolecular
phylogenies(Doyle2007).Theinferredancestralvenationwaspinnate,asinmostlowerPotomac
308 Doyle
EA40CH13-Doyle ARI 23March2012 14:10
angiosperms,buttherewerethreeearlyoriginsofpalmatevenation,inNymphaeales,Piperales,
andeudicots,consistentwiththepresenceofafewpalmatelyveinedleaftypesinthelowerPotomac
andtheirincreasingdiversityintheupperPotomac.Upchurch(1984)notedthatstomatalpatterns
inlowerPotomacleavesweremostlikethoseinAmborellaandAustrobaileyales,15yearsbefore
thesetaxawererecognizedasbasal.
Most phylogenetic analyses of Early Cretaceous angiosperms (see Figure 3) have involved
fossilflowers.Someofthebest-studiedlocalities,fromPortugal,wereoriginallythoughttobeas
oldasValanginian,butmorerecentcorrelationsimplythatmostofthemarelateearlyAlbian,
withTorresVedrasprobablybeingolder(seeSupplementalSection1;followtheSupplemental
MaterialslinkfromtheAnnualReviewshomepageathttp://www.annualreviews.org).Original
descriptions of taxa that have been analyzed phylogenetically are referenced in Supplemental
y. Section2.Mostofthesefossilsappeartobelongonthestemlineagesoflivingfamiliesorlarger
nl
go clades(seeSupplementalSection3).
s.oruse PhylogeneticanalysesshowbetterevidenceforMagnoliidaeandotherbasalgroups,beginning
viewonal beforeandcontinuingalongsidetheradiationofeudicots.Doyle&Endress(2010)confirmedand
annualreFor pers mreafinnieadn)cowmithpaMrisaognnsoolifaElens,drVeisrsigniinaia(nlattheuAs(pmtiiadnd,lBerAazlbili)aann)dwAitrhchbaaesaanltLhuausr(laalteesAanlbdiaMn–aeualdrliyniCae(lnaote-
w.2. Albian–early Cenomanian) with Lauraceae and Hernandiaceae, and Walkeripollis pollen tetrads
w1
w1/ (lateBarremian–earlyAptian)withWinteraceae.MonocotsarerepresentedfromtheAptianon-
om 05/2 wardbyLiliaciditespollen,withdiagnosticgradedsculpture(Doyle1973,Walker&Walker1984,
d fron Doyleetal.2008);byAcaciaephyllum,aleafystemwhoseassignmenttomonocotswasquestioned
Downloadeomonosov bnthyeeaGrA-abNnadIsToallAfmogoertnaaodlce.o:(2tM0fa0omn0e)itlbiyaunAttrchaoucnsefi(aeream(rFleyrdiAibslybeDitaanol).y2lien0e1Nt0ayblm)..(pA2h0ta0lee8aa)c;setaantewdo(bFyflrioiinwsfleeotrrsaelas.rc2ee0ns0ec9ceu)srraeenlldyatpAeldnacatoecodtsthiinea
26. of L (early-middleAlbian)inAustrobaileyales(Doyleetal.2008).OtherprobableNymphaealesare
0:301-3Library PJolurdriacnar(pTelalaytlioarfertoaml.t2h0e08la).te Aptian of Brazil (Mohr et al. 2008) and leaves from the Albian of
ci. 2012.4Scientific aenuddDicpooaytlmlelian&teesEl:ynpldeorlbetaestsde(2aln0ead1v0ep)sianlansnoadtceoflyrnufidirtismssoeefdctNaefdefilnuleimtaivbeeistseos(fpwmlaiittdhadnNloeiedaluns,mdSblaaot,peihnAedalobdpissaisno)ftwauxitnahiwsPeitxlhautatalrniflcuoso,lwpaaentrdes
Earth Planet. Se University - AtCuhnlrebiesitteaarxnciuc-eCoaolluepSsnoporNaamntooearmnmpieaoranalploeflbnloolewutsyneppdreosaslrwlyetihnt(haBttaBosbuiFenxgagaigcenaerlate&eos.ipDTsrhiowlecleihffilelerrresats1ttefl9ao8binr4lia)sl,thhebeevuditdlbaettyhneecaAyesslmfobociaraiyanPt.bieoTennthraeweppeirrttheealslaaeftoenisotisesnidlnofleafoamrLwotaenhtrgees
ev. Stat (Friis1984,Friisetal.2006b).
Rw
Annu. Mosco lumFiofstshilessreefloatremdtaoctlhadeen)oawre-orbemscuarrkeafbalmyiclyonCshpliocuraonutshianceeaaerl(yoranCghiolospraenrmthaflcoeraaesp.lTuhseCseeraintocplhuydle-
y monosulcatepollenwithcharacteristicsculptureandathicknexine(Clavatipollenites,Asteropollis,
b
Pennipollis: Doyle 1969, Walker & Walker 1984, Doyle et al. 2008), leaves with chloranthoid
teethandstomata(Upchurch1984),andextremelysimpleflowerswithsingleuniovulatecarpels
(Pedersenetal.1991,Friisetal.2000,Eklundetal.2004).SomehavesuggestedthatChloran-
thaceae offer an alternative prototype for the angiosperm flower (Nixon et al. 1994, Taylor &
Hickey1996),butthisconflictswithmoleculardata,whichplacethefamilysecurelyinthemesan-
giosperms,implyingthattheirfloralsimplicityisaresultofreduction(Endress&Doyle2009).
Thisviewisconsistentwiththecoevalexistenceofmorecomplexflowersandisfurthersupported
by Canrightia (Friis & Pedersen 2011), which resembled Chloranthaceae and Ceratophyllum in
havingoneorthotropousovulepercarpelbutretainedbisexualflowerswithseveraltepals,sta-
mens,andcarpels.AlthoughChloranthaceaemaynotbeakeytotheoriginofangiosperms,they
www.annualreviews.org • OriginofAngiosperms 309
EA40CH13-Doyle ARI 23March2012 14:10
aresignificantasthefirstcommonangiosperms,whichbearsonecologicalcausesfortheriseof
thegroup(Feildetal.2004,Feild&Arens2007).
SimilardiscussionwasstimulatedbythefindingthatHydatellaceae,minuteaquaticplantswith
linearleavesthatwereassumedtobemonocots,areinsteadabasalbranchofNymphaeales(Saarela
et al. 2007). Their reproductive structures have been interpreted as inflorescences of unisexual
flowers consisting of one stamen or one carpel, but Rudall et al. (2009) suggested instead that
theyrepresentanonfloralorprefloralstate.However,thephylogeneticpositionofHydatellaceae
impliesthattheirflowersarereduced(Endress&Doyle2009).
ArelatedcaseisArchaefructus,anaquaticplantwithfinelydissectedleavesandreproductive
axesbearingsingleorpairedstamensandcarpels,fromtheYixianlakebedsofnortheastChina
(Sun et al. 1998, 2002). Archaefructus was first reported as the oldest known angiosperm (Sun
y. etal.1998),becausetheYixianwasthoughttobeLateJurassic,butthebedshavebeenredated
nl
go radiometricallyasBarremianorAptian(Zhouetal.2003).AcladisticanalysisbySunetal.(2002)
s.oruse placed Archaefructus below all living angiosperms, which led them to suggest that it illustrates
viewonal a prefloral stage before the perianth, stamens, and carpels were grouped into typical flowers.
annualreFor pers Hthoatwtehveerr,eFprroiidsuecttailv.e(2a0x0es3)wceitreedinthfleorfaecstcethnactesthoefsrteadmuecnedsaunndisceaxrupaellsflaorweeorfst.eTnhineypaailrssoansoetveiddetnhcaet
w.2. the ternate pattern of leaf dissection resembles that of Vitiphyllum in the lower Potomac and
w1
w1/ Ranunculalesintheeudicots.PhylogeneticanalysesbyDoyle(2008)andEndress&Doyle(2009)
om 05/2 nestedArchaefructusintheangiospermcrowngroupwithoneoftwotaxathathaveevensimpler
d fron flowers,dependingonthebackbonetree:Ceratophyllum,ifthisplantislinkedwitheudicots,or
Downloadeomonosov Hppooylldlleeannt,eglblrauacitneFase.ri.IifsTpehotelalseel.nr(ec2hs0ua0lr3tas)cdqteeurpesesotnifdoAnoerncdhtawhehefreudtchetseucrsraitphreteiosrcneomoreafdiAnasrscfihuganeukfrrneuodctwubnsy,aSistushnmaveoitnsatglp.ma(2ros0ni0mo2so)unwlicoeaurtees
26. of L positionisinRanunculales(Endress&Doyle2009).Underanyofthesehypotheses,Archaefructus
0:301-3Library istoTohfeasrefraonmd oththeebrafsoesosiflsthweitahngeiuodspiceortm-lsikteofheaavteuraesmpaojosreipmrpoabcletmonsifnofrerthreedcaonncgersutreanlcsetaotefst.he
ci. 2012.4Scientific la2es0as0of,6c,piaSotulelndenew,tiaatnhl.d2eu0fl1do1iwc)oe.rtV-rliitekicpeohyrfodlluus.rm-ToahncecduYfirisvxweia-inctahFrtpoherelmloaatltedieofsrntutiartlsisco(oSlciponanotcetaarpipnouslsl,esinLmeipneflretuhacetnuPdso:ttLeoremnnaagtce&(DleFoarvyieliess
Earth Planet. Se University - &2Ab0up0tHti6oai)nnc,klbyoeuyfitsAo1thl9fare7tice6Yad,ixHapinariednc-kiASesoylBbu&aitarhnrDeAtmormiyicaleoenrlip1oca9art7eA(7Dgp),rtoiaayaitlnnea.sT1lae9rrve9iec2klo,ntlBphoaawrtetnenispninoperlrEloe1ubn9rao9obp6cly,ecuH(erHaseruiilmnigehthshteoesAfe1llarb9ti&9eas4nt)H,B(Haoanrcodrhceuhnmluoiilra2itnh0e1etaa0nas)dlt,.
ev. Stat China was at a higher paleolatitude, where tricolpates generally appeared later (Brenner 1976,
Rw
Annu. Mosco Hpoilclkeenyin&thDeoAypletia1n97o7f,ACrgraennetin&a(LAirdcghaarndg1e9ls8k9y).etTael.rn2a0t0e9ly,Ploubeebdlal2ea0v0e9s).aOlsoneppreodssaitbeiltirtiycoislpthataet
y someoralloftheseleavesarenoteudicots,butratherextinctlinesofNymphaeales,asproposed
b
forArchaefructus.Anotheristhattheyrepresenttaxaontheeudicotstemlineage,beforetheorigin
oftricolpatepollen.ParsimonyanalysisimpliesthatdissectedleavesarosewithinRanunculales
(Doyle2007),butaccordingtolikelihoodanalysis(Geetaetal.2012)theyprobablyalreadyexisted
intheancestorofeudicots.Alternatively,itmaybethattricolpatepollenoccursintheYixianand
Argentina but is rare because the first eudicots were low pollen producers. Wang et al. (2000)
reported“prototricolpate”pollenfromtheYixian,butitisnotclearthatthesegrainshavethree
colpi;atleastone(figure21ofWangetal.2000)maybeacrushedgrainoftheconiferClassopollis.
An important result of molecular studies concerns the original morphology of the carpel
(Figure 3). The ANITA rooting refutes the older view that the ancestral carpel was plicate
(conduplicate),likealeaffoldeddownthemiddleandsealedbyfusionofthemargins,asinsome
310 Doyle