Molecular and Fossil Evidence on the Origin of Angiosperms - Index of

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
James A. Doyle
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alreviee only. email:[email protected]
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2012.de Ev Annu.Rev.EarthPlanet.Sci.2012.40:301–26 Keywords
ci. de TheAnnualReviewofEarthandPlanetarySciencesis Cretaceous,molecularsystematics,paleobotany,palynology,phylogeny
Earth Planet. Son: Universida oT1C0noh.lp1iisn1year4ri6agtt/ihcaetlnea(cid:2)n’rcstuhdr2.eoa0vin1:-n2euabraytlhrAe-v0ni4ne2wu7as1l.o1Rr-eg1v0i5e3w1s3. AMthbeoislretcrinuaclcartreadsaintagomnorreplahtoiolongsihciaplsdwiviethrsinityanthgrioosupgehrmthsecoCnrfietramcetohuesvrieeflwecttheadt
Rev. by b- Allrightsreserved their evolutionary radiation. Despite the early appearance of aquatics and
u. 0084-6597/12/0530-0301$20.00 groups with simple flowers, the record is consistent with inferences from
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A moleculartreesthatthefirstangiospermswerewoodyplantswithpinnately
veinedleaves,multipartedflowers,uniovulateascidiatecarpels,andcolumel-
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
raisequestionsabouttheinterpretationofbothlinesofevidence.
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or Thisreviewexploresareasofcongruenceandconflictandwaysinwhichconflictsmightbe
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ualreviese only. tleiomnawroyudlidveinrvsiofilcvaetpiornim,eamrilpyhaansiuznindgerasptahnydloinggenoefttihcefroarmigeinwoofrkth.eAdsiustcicnecstsifvuelnsoewlutiniotnrintositchfeeaptruorbe-s
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anal ofangiosperms,orsynapomorphies,bytransformationofstructuresknowninrelatedplants,and
ww.son secondarilyanunderstandingofextrinsicaspects,suchaswhenandwherethesechangesoccurred
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01-UE andothergroupsandthecharacteroftheearliestangiospermrecordintheBarremian,Aptian,
40:3ora ( andAlbianstagesoftheEarlyCretaceous.Therecordthenconsistedlargelyofleaves,whichhad
12.Ev beenidentifiedorcomparedwithdiversemoderntaxa.Theresultingimpressionthatangiosperms
20de appeared“suddenly”in“modernform”ledtosuggestions,goingbacktoDarwinin1879(Friedman
ci. de 2009),thatthegrouporiginatedanddiversifiedbeforetheCretaceousinsomeareawithapoor
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arth Planet. n: Universid faoonfsgdsiieolpsropesecirotmirodsn.oiTrnihgtehinebaeCtesrtdeditnaecvteeroolouppsiceaadsltauhpreeloasnruydltswoianfsitnthhceraePtaeosrifmnAgixlayenleroqorudTa(br1li9eas5cs2liic,m1aan9t7de0si.)n,vwadheodploowstlualnadtebdatshinast
Eo This picture began to change with studies of fossil pollen, which provided evidence on flo-
Rev. by b- ras in geographic areas where plant megafossils were unknown and broader representation of
u. taxamakingupthevegetation.Despitenearlyworldwidesampling,palynologicalstudiesfailed
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A torevealangiospermpollenbeforethemid-EarlyCretaceous,whereas someshouldhavebeen
transportedfromtheuplandsifangiospermsweregrowingthere,andfoundthatEarlyCretaceous
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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Eo Gondwana), but there, too, they were preceded by monosulcates (Brenner 1976, 1996; Doyle
Rev. by b- etal.1977;Schrank1983;Penny1986;Regali&Viana1989;Doyle1992;Ibrahim2002;Schrank
u. &Mahmoud2002).TricolpateswerejoinedinthelateAlbianbytricolporatepollen,themost
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A common type in living eudicots, with a pore in the middle of each furrow. Tricolporates were
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,
with unusually irregular venation. Similar features occur in Recent “woody magnoliid” groups
g withmonosulcatepollen.Afewarepalmatelyveined,asin“herbaceousmagnoliids.”Ternately
or
s. dissectedleaves(withthreefolddivisionoftheblade),asintheeudicotorderRanunculales,appear
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annal u blewithlivingtricolpategroups,suchaspeltateleaves(Nelumbites)similartotheaquaticgenus
w.on Nelumbo(lotus),palmatelylobed“platanoids”comparedwithPlatanus(sycamore),andpinnately
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d from 2. For p eCtoanl.si1st9e9n3t).seMquoestncoefsthaereseklneoavwenshinavweemstoerrnerNegourltahrAvemneartiicoan,tPhoarntutghaols,eKinaztahkehsltoawne,rCPoolotommbaiac,.
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01-UE withotherseedplants.However,theydidhelprefuteoldertheoriesbasedonderivedtaxa,such
40:3ora ( as comparisons between Fagales and Gnetales, and favored those based on angiosperms with
12.Ev monosulcatepollen(Doyle1978).Mostdiscussionsoftheorigincenteredonso-calledMesozoic
20de seedfernssuchasglossopterids(actuallyPermian),corystosperms(Triassic),andCaytonia(mainly
ci. de Jurassic),andpossiblehomologiesoftheouterintegumentofthebitegmicangiospermovulewith
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arth Planet. n: Universid tDhielBcsheeegeridn1-nb9ie8na1gr)i.inngthcuep1u9l8e0os,futhnedseersttaaxnad(inGgauosfstehne1C9r4e6ta,cSetoeubsbiannsgi1o9s7p4e,rmDoreycleor1d9w78a,sRfuerttahllearcrkev&-
Eo olutionizedbydiscoveriesoffossilflowersandfruits(Friis1984;Friisetal.2000,2006a,2010a,b,
Rev. by b- 2011),mostlyinthemesofossil(millimeter)sizerange.Contrarytoearlierassumptions,flowers
u. are often well preserved as lignite or charcoal and can be extracted from sediments by sieving
n
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A andstudiedwithscanningelectronmicroscopyorX-raymicrotomography(Friisetal.2009,Friis
& Pedersen 2011). Flowers have been the mainstay of angiosperm systematics since Linnaeus,
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
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01-UE wherethecrowngrouptreeisrooted,orwhichextantlinesaremostbasal(attachedtothemost
40:3ora ( basalnodes).Basaldoesnotnecessarilymeanprimitive:Livingrepresentativesofbasallinesare
12.Ev usuallymoreorlessspecializedrelativetothelong-deadcommonancestor(Crisp&Cook2005).
20de However,giventhecharactersoflivingtaxaandthetreetopology,wecanusetheprincipleof
ci. de parsimony(orrelatedcriteria)tooptimizecharacterstatesonthetreeandestimatetheancestral
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arth Planet. n: Universid seatxcaaltmaed,peel,veei,tniifsitnmhteohrseetaapbraesretsnwimcoeooonrfiomduaotsarteofrlorinemecosonwustittgrhruotchutepthssia(samstteoapstet-adatoeswabnnracanepscpthrriaonla.gcTihnh;eBasaseetecrmioensadnbpeelrtooawbl.lte2hm0e0bi6su)w.lkFhooartf
Eo theclosestoutgroupsoftheangiospermsare(thenearestbeingthesistergroup).Again,outgroups
Rev. by b- maybemoreorlessderived,butifseveraloutgroupsareknown,itmaybepossibletoreconstruct
u. characterstatesatnodesbelowtheangiospermsandinferhownewangiospermfeaturesevolved
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A fromstructuresknownintheoutgroups(abottom-upapproach).Thesequestionsinvolvearisk
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
to the Cretaceous radiation because its interpretation is essential for reconstructing ancestral
g statesandgainingperspectiveonconflictsbetweenmolecularandfossilevidenceontheageof
or
s. angiosperms.
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01-UE Amborella,ascramblingtreeorshrubinNewCaledonia;Nymphaeales;andAustrobaileyales,a
12.40:3Evora ( cfolardAemofbloiraenllaas,,Nshyrumbpsh,aaneadlessm,aIllllitcrieaeles,s,thTermimoesntiafa,manildiarAbuestinrogbaIlilliecyiau.m) T(shtaerraenmiseai)n.(iAngN>IT9A9.9st%andosf
20de angiospermspeciesformacoregroupnamedmesangiosperms(Cantinoetal.2007),madeupof
ci. de fiveclades:Chloranthaceae,notedfortheirsimpleflowers;Ceratophyllum;Magnoliidae,inanew
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arth Planet. n: Universid mapnoodllnePonpi.phWeyrlaietltehiscin(sieennucsdlueic,doicntosgn,sRAisratinisnutognlcooucflhaMilaeacsge(anpeoo)l;piapmlieeossn,,oLbcuaoutttrsea;rlacenus,dpCse)auandneidclloastecsev,aewerai(tlihnoctthrluiecdroillnipngaetWsefaoinnrtdmerdaaecrbeiaavseea)dl,
Eo gradewithmostlytricolpatepollenbelowavastcorecladetermedPentapetalae,mostofwhich
Rev. by b- havepentamerousflowerswithaperianthdifferentiatedintofivesepalsandfivepetals,aswellas
u. tricolporatepollen.
n
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A Somemolecularresultsthatcontradictedolderviewswereanticipatedbymorphologicalanal-
yses, such as the monophyly of eudicots and the association of Aristolochiaceae with Piperales
(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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artn: fossiltaxaplacedatmostparsimoniouspositionsbasedonanalysesofDoyleetal.(2008),Endress&Doyle(2009),Friisetal.(2009),
Rev. Eby b-o Dfoormyl.eP&roEbnabdlreespso(s2it0i1o0n)s,oanfdotFhreirism&onPoecdoetrsseannd(2e0u1d1ic).oCtsoalroersinodfibcaratendc.hCesoilnodrsicbaetehitnhdenmaomsetspoarfsfiomssoinlsioinudsiccoauterssetroaftiegvroapluhtiiconpoosfitciaornpsel
u. oflocalitieswheretaxaoccurorhavebeendescribedinmostdetail.DrawingofalongitudinalsectionofanascidiatecarpelofTrimenia
nn providedbyP.K.Endress.
A
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
below)(Endress&Doyle2009).ThetwoarrangementsofAmborellaandNymphaealeshavelittle
g impactontheseinferences.
or
s. TherelationoftheseresultstotheCretaceousrecordcanbeevaluatedbyoptimizingindividual
w
alreviee only. clihvainragcttaexras.oTfhfoesisdilesalonapaprmoaoclehcmuliagrhttrebeeoartobtyalaenvaildyeznincgeaandaalytasisse(tHtehramtisnecnlu&deHsebnodtrhicfkosss2il00an8)d,
us
annal u withadatasetofmorphologicalcharactersforbothlivingandfossiltaxaandmolecularcharacters
w.on for living taxa, but so far moststudies have used a molecular scaffold approach (Springer et al.
ws
wer 2001),inwhichamorphologicaldatasetforlivingandfossiltaxaisanalyzedwiththearrangement
d from 2. For p o20f0li8v,inFgritiasxeatfiaxl.e2d0t0o9a,Dbaocyklbeo&neEtnrederebsass2ed01o0n,Fmroiilsec&ulPareddeartsae(nE2k0lu1n1d).eTthails.2se0e0m4,sDjuosytilfieeedtoanl.
e1
26. Downloadora) on 09/05/ trbhouebtMugthsroteolesueencnuoadslusasgruthhmraetpthstuafioolttsnstshsiclessohanhodfiaudvrliemdtirobetnehlaatotetifvsttefheolydessfiisneltswrtawhtcieohgufraulardtpauchprtireeco.rbsoarabdnledyrtnohofattaampffpoeecsattramthnoecleetocopufolaalrongrgeyiolaostpfioelinrvmsihnigppostallaxerane,
3v
01-UE types corresponds to their sequence of evolution (Doyle 2005, 2009). The inferred ancestral
40:3ora ( aperture state is monosulcate, as in the oldest recognizable angiosperm pollen. Prior to the
12.Ev ANITArooting,a continuous tectumand granular exine structurewere widely considered an-
20de cestral.FossilpollenwiththesefeatureswouldbedifficulttodistinguishfrompollenofBennet-
ci. de titales and might therefore have existed long before the Cretaceous without being recognized
Sa
arth Planet. n: Universid (toMhuesu,alalnercreet1sit9cru7al0la,teeDxitoneyeclteustmertuacartluo.rs1ee97awt5at,shWeconalloukdmeerec&lolanrWn,eaacnltkdienragl1tAh9u8os4ut)gr.ohHbtaohilweeeytvaeelcerts,uammnodwlemacsuesloaarrniggtriinoeeasplsleyimrmcposln.ytTitnhhuai-st
Eo suggeststhatValanginianreticulate-columellarmonosulcatesmaynotbeasfarfromtheorigin
Rev. by b- of angiosperms as thought. The continuous-tectate stage may be represented by Hauterivian
u. pollenwithaverrucatetectumreminiscentofAmborella(Hughes1994;Doyle2001,2005;Hesse
n
n
A 2001).
Molecular trees imply that tricolpate pollen, the next major fossil type, evolved once from
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 Supplemental Material
MaterialslinkfromtheAnnualReviewshomepageathttp://www.annualreviews.org).Original
descriptions of taxa that have been analyzed phylogenetically are referenced in Supplemental
Section2.Mostofthesefossilsappeartobelongonthestemlineagesoflivingfamiliesorlarger
g clades(seeSupplementalSection3).
or
s. PhylogeneticanalysesshowbetterevidenceforMagnoliidaeandotherbasalgroups,beginning
w
alreviee only. breefifonreedacnodmcpoanrtiisnounisngofaElonndgrseisdsienitahe(laratediAatpitoinano,fBeruadziicl)oatsn.dDAoryclhea&eanEtnhudsre(lsast(e2A01lb0i)acno–nefiarrlmyeCdeannod-
us
annal u manian)withMagnoliales,Virginianthus(middleAlbian)withbasalLauralesandMauldinia(late
w.on Albian–early Cenomanian) with Lauraceae and Hernandiaceae, and Walkeripollis pollen tetrads
ws
wer (lateBarremian–earlyAptian)withWinteraceae.MonocotsarerepresentedfromtheAptianon-
d from 2. For p wDaorydlebyetLaill.ia2c0id0i8te)s;pboylAlecna,ciwaietphhydlilaugmn,oastliecagfyrasdteemdswcuhlopsteuraess(iDgnomyleen1t9t7o3m,Wonaolkcoerts&wWasaqlukeesrti1o9n8e4d,
e1
26. Downloadora) on 09/05/ bnt(ehyeaeaGrrlA-yabN-nmadIsToaidllAfdmolegoertnAaaodllbce.oi:(a2tMn0f)a0omin0ne)itlbAiyauunAtstrtchraouocnsbefi(aaereialme(rFyleyardliAeibsslybe(DitDaanool).yy2lilene0e1Net0taybalm).l..(pA22h0t0a00lee88aa))c;s.teaOantewdtho(bFeyflrrioiipnwsrfleoeotrbrsaaelabs.rcl2eee0nsN0ec9ceyu)smrarepenllhdyaatpAeeladnalcaetoecsodstathriineae
3v
01-UE Pluricarpellatia from the late Aptian of Brazil (Mohr et al. 2008) and leaves from the Albian of
40:3ora ( Jordan(Tayloretal.2008).
12.Ev Doyle&Endress(2010)alsoconfirmedaffinitiesofmiddleandlateAlbiantaxawithtricolpate
20de eudicot lines: peltate leaves and fruits of Nelumbites with Nelumbo, heads of unisexual flowers
ci. de and palmately lobed and pinnately dissected leaves (platanoids, Sapindopsis) with Platanus, and
Sa
arth Planet. n: Universid Atuhnlebisitearxniuc-CoallepSnoporaamntoeamnpieaornalleflbnoowutynepdresasrwytiht(haBtaBsbuienxggaicenerat&eo.pDTrhioleclihffieerrrsat1tefl9o8inr4a)l,thebevuitdlaetthneecAyelmfboiaraynP.beTenthraeepperrteealslaaeteniotiesndnoeafamrLotanhtgee
Eo Cretaceous Normapolles pollen to Fagales is well established by association with fossil flowers
Rev. by b- (Friis1984,Friisetal.2006b).
u. Fossilsrelatedtothenow-obscurefamilyChloranthaceae(orChloranthaceaeplusCeratophyl-
n
n
A lumiftheseformaclade)areremarkablyconspicuousinearlyangiospermfloras.Theseinclude
monosulcatepollenwithcharacteristicsculptureandathicknexine(Clavatipollenites,Asteropollis,
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
etal.1998),becausetheYixianwasthoughttobeLateJurassic,butthebedshavebeenredated
g radiometricallyasBarremianorAptian(Zhouetal.2003).AcladisticanalysisbySunetal.(2002)
or
s. placed Archaefructus below all living angiosperms, which led them to suggest that it illustrates
w
alreviee only. aHporweeflvoerra,lFsrtiaisgeetbale.f(o2r0e0t3h)ecipteedritahnethfa,cstttahmatenthse, satnadmceanrspaenlsdwcaerrpeelgsraoruepoefdteninitnoptayiprsicaasleflviodweenrcse.
us
annal u thatthereproductiveaxeswereinflorescencesofreducedunisexualflowers.Theyalsonotedthat
w.on the ternate pattern of leaf dissection resembles that of Vitiphyllum in the lower Potomac and
ws
wer Ranunculalesintheeudicots.PhylogeneticanalysesbyDoyle(2008)andEndress&Doyle(2009)
d from 2. For p nfleoswteedrsA,drcehpaeenfrduicntgusoinntthheeabnagckiobsopneermtrecero:wCneragtroopuhpyllwuimth,iofntehiosfptlwanottaisxalinthkaetdhwaviteheevuednicsiomtsp,loerr
e1
26. Downloadora) on 09/05/ Hpppoooyllsdllieetainnto,englblriauascitinenFase.Rri.IiafsTnpeuhotnelalsceelu.nlr(aec2lehs0usa0lr(3tEas)cndqtdeeurrpeseessotnsifdo&AnoerDncdhotawyhelhefereud2tche0tse0ucr9sr)ait.phrUeteionsrcnedomeorreafadiAnnasyrscfiohugfaneutkfhrrneeuosdcetwubhnsyy,apSistoushtnhmaeveositnesatsgl,p.Ama(2rrocs0hni0mao2esof)urnwuliccoeaturuteess
3v
01-UE istoofarfromthebaseoftheangiospermstohaveamajorimpactoninferredancestralstates.
40:3ora ( These and other fossils with eudicot-like features pose problems for the congruence of the
12.Ev leaf, pollen, and flower records. The Yixian Formation also contains simple and ternate leaves
20de associatedwitheudicot-likefour-andfive-carpellatefruits(Sinocarpus,Leefructus:Leng&Friis
ci. de 2006,Sunetal.2011).VitiphyllumoccurswiththeoldesttricolpatepolleninthePotomac(Doyle
Sa
arth Planet. n: Universid &2A0p0Hti6ai)nc,kboeuyftA1th9fre7ic6Ya,ixHainaidnckiSesoyBu&atrhrDeAmomyialeenri1oc9ar7A(7Dp),toiayatlnea.T1le9rv9iec2lo,tlBphaartetenispnoperlrloe1bn9a9ob6cly,cuHeraseriilmniethshtoeAfellarbti&easntHB(Hoarcorhceuhmluiila2in0e1ta0na)dl,.
Eo butonlyisolatedpre-AlbiantricolpategrainsareknowninEurope(Hughes1994),andnortheast
Rev. by b- China was at a higher paleolatitude, where tricolpates generally appeared later (Brenner 1976,
u. Hickey & Doyle 1977, Crane & Lidgard 1989). Ternately lobed leaves also predate tricolpate
n
n
A pollenintheAptianofArgentina(Archangelskyetal.2009,Puebla2009).Onepossibilityisthat
someoralloftheseleavesarenoteudicots,butratherextinctlinesofNymphaeales,asproposed
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