Copyright (c) American Society for Taxonomists. All rights reserved. Delivered by Ingenta to IP: 192.168.39.211 on: Sun, 03 Oct 2021 00:44:52 DOI 10.1600/036364411X553216 © Copyright2011 bythe American SocietyofPlantTaxonomists Systematic Botany biogeographic relationships amonglineages. hypotheses ontheevolutionofgrowth formsandexamine geographically diverserepresentatives ofbothgenera,totest characters usedtoseparate these results haveimplications fortheevolutionoffloral Byttneria 2001 ) suggestedthatall included fivespeciesof tats. A phylogenetic analysisofthechloroplast gene both genera are mostdiversein tropical forests, intheNewWorld, or, inthecaseof tropical regions, andmaybesubshrubs, shrubs, smalltrees cal. Speciesofbothgeneragrow inwarmsubtropical and Ayenia diversity ofgrowth forms foundinthetwogenera.While their tinyyetextraordinarily complexflowers,aswellthe rate theapproximately 135speciesof ied inthesespecies. Androecium and petalmorphologysepa- although pollinationbiology hasapparently notbeen stud- associated withflypollination ( Faegri andvanderPijl1971 ) from somespecies( Cristóbal 1960 , or purplishcoloration,smallsize, andthefetidodorreported 1976 ) are allgenerally staminal column.Themorphology oftheflowers,theirreddish of thepetal,from thepointofinsertiontowhere itrejoins the ogy of Dorr (1996) anduse“claw”torefer tothenarrow base (see Dorr 1996 andreferences therein). We followtheterminol- and “lamina”maybeapplieddifferently bydifferent authors lenging todescribeandcommonterminologysuchas“claw” appearance. Thecomplexityofpetalformhasproven chal- 1976 , 1981 ). Thismorphologygivestheflowersalantern-like concealing minuteantipetalousanthers( Cristóbal 1960 , 1965 , arch uptorejoin thestaminalcolumnatitsapex,partially “clawed,” petalsthatinsertatthebaseofandroecium and gates analyses of ogy. Here, wepresent theresults ofexpandedphylogenetic indicative ofphylogeneticrelationships thanfloralmorphol- ingly suggestthatbiogeographyandgrowth formsare more Te hlgn o of Phylogeny The Ayenia Byttneria shrubs, and lianas.Here, wereconstruct relationships among37speciesof the evolutionofgrowth forms. seasonal, openhabitats. Additional samplingof African speciesof we recovered areversal from semi-scandentshrubs tofullyuprightplants.Within theneotropics, there are twoindependentrad to spiny, semi-scandentshrubs occurred intheneotropics. We foundnoevidenceoftransitionsfrom lianastoanyothergrowth sition tounarmedlianas,withsubsequentradiationsintothe Asian and African tropics. A secondindependenttransitionfrom t combined Rayleya resulting phylogenytotesthypothesesontheevolutionofclimbingplantsandexaminebiogeographytheseplants.Results Ayenia Rayleya isrestricted totheNewWorld, Abstract— Keywords— , sistertoneotropical speciesof and issistertoacombinedcladeof and and (2011), 36(1):pp.129–136 Ayenia and Ayenia/Byttneria/Rayleya 2 Byttneria Tropical plantsshowadiversityofgrowth forms,yetfewphylogeniesare availabletoexaminethetransitionsbetweentrees, Ayenia Department ofBiologicalSciences,Texas ChristianUniversity, FortWorth, Texas 76129,U.S. A. Byttneria yteia yteiiee, boegah pN ins, toia . tropical lianas , cpDNA, biogeography , , Byttnerieae, Byttneria Megatritheca and 1 havelongfascinatedbotanistsdueto Department ofBiology, UniversityofMiami,CoralGables,Florida33124,U.S. A. Byttneria , togetherwiththerecent segre- Ayenia Ayenia haveradiatedintodry, openhabi- , lianas. Although speciesofboth Ayenia Ayenia , haveunusualconstricted,or and sampledwere nestedwithin , withmorphologicallyand cladeisreconstructed asaneotropical tree orshrub. Within the and

3 Byttneria , , Author forcorrespondence ( [email protected] ) Ayenia Byttneria Byttneria, abr A Whitlock A. Barbara Byttneria Byttneria Byttneria the EvolutionofGrowthForms and Communicating Editor:Andrea Schwarzbach ( Whitlock etal. from the ca.70 Byttneria , andintrigu- ispantropi- . Ifupheld, and ndhF ; ; Byttneria that Rayleya Byttneria 1 isparaphyleticwith 129 , 3 n mna . Hale M. Amanda and to eithergenusascurrently circumscribed. but includespeciesthatcannotbeassignedwithconfidence Rayleya (1965 , 1981 ) describedtwosmallgenera, androgynophore isoftenbarely discernible. umn. Similarappendagesoccurinsome the abaxialsurfacewhere thepetalsrejoin thestaminalcol- ages (see Dorr 1996 foradiscussionoftheterminology)on cies generallyhaveprominent ligulesorprojecting append- width asitmeetsthestaminalcolumn.Petalsin in in genera alsodiffer inthedegree ofconstrictionthepetalclaw: nophore of Byttneria and pronounced petalappendagessimilartothosefoundin species from southeasternBrazil,hasfivedithecateanthers small sizeof androgynophore thatislackingin are usuallyinconspicuous. Flowersof anthers in usually interpreted ashaving fivestamens,withdithecate revisions ofthegenera( Cristóbal 1960 , 1976 ). Bothgeneraare species of tropical Africa, whereas whereas tropical Africa, tion, bothspecies of expanded apex,andaprominent abaxialappendage.In addi- is similartowhatseenin well assomenovelcharacters. Thepetalclawof features usuallyassociatedwitheither Rayleya cies previously placedin Ayenia lar hairsfoundatthebaseofsepalsinsome similar functioninpollinationtothesmalltuftsofglandu- Cristóbal hypothesizedthatthisprotuberance mayservea on theadaxialsurfaceofpetalsatpointinsertion. (see below),inhavingapresumably glandularprotuberance from allspeciesof Ayenia, Byttneria, mayyieldmore complicatedscenariosinbothbiogeographyand In thecourseofherworkwith The Ayenia, Byttneria (Malvaceaes.l.)anditsImplicationsfor species. , thatare clearlycloselyrelated to , thetwospecies of , butthedelicate,narrow petalclawsandandrogy- thepetalisnarrow formostofitslength, whereas Ayenia Byttneria thepetalisnarrow atthebasebutexpandsin Ayenia Megatritheca Ayenia Ayenia and , aswelldelimitsectionsinthemostrecent Byttneria

(Citbl 91) 1981). (Cristóbal nestedwithinit.Thecommonancestorofthe andtrithecateanthersin Rayleya flowers(usually Megatritheca Ayenia/Byttneria 2

Ayenia consistsoftwoCentral African spe- withcpDNA sequences,andusethe Megatritheca Byttneria and Byttneria isrestricted tothe Americas. Byttneria Ayenia , likesome clade,there isasingletran- (Citbl 95) A with As 1965). (Cristóbal Byttneria. , withaconstricted base, Rayleya bahiensis < Ayenia , aswell showacombination of 1cmindiameter),the Byttneria and Byttneria Ayenia Byttneria Rayleya, form; however, Megatritheca alsohavea short Ayenia rees orshrubs Ayenia Becauseofthe iations into showthat Byttneria or Byttneria speciesbut Megatritheca Megatritheca and , Cristóbal , Ayenia, withone . Thetwo , occurin differs Ayenia and spe-

and as

Copyright (c) American Society for Plant Taxonomists. All rights reserved. Delivered by Ingenta to IP: 192.168.39.211 on: Sun, 03 Oct 2021 00:44:52 3 SSEAI OAY [Volume 36 SYSTEMATIC BOTANY all speciesof Megatritheca However, asthenameofgenussuggests,stamens 130 Approximately 60species of of eight m)withawell-definedtrunk ( Cristóbal 1960 ). Species species of malvaceous palmately-veinedandtoothedleaves.Onlytwo be lowwithprocumbent ordecumbentbranches,typically cies of are erect, orself-supporting,shrubs orsmalltrees. Mostspe- well as tions betweenforms.Manyspeciesof vide abaselineforinvestigationsintoevolutionarytransi- she recognized withinbothgenera.Theseobservationspro- correspondences betweengrowth formsandthesections that emphasize vegetativecharactersinherrevisions, shenoted Byttneria tecture, functionalmorphology, andecologyin true formosttropical plants,detailedstudiesonthearchi- extent in ous staminodesasinothergenera). bearing partsofthestaminaltube(ratherthanantisepal- so thatthepetalapicesare adnatetotheantipetalousanther- developed staminodesthatare belowthelevelofanthers oblong anthers(vs.smallandsuborbicular),thebarely other Byttnerioideaeare mostlytricolporate),large and stigmas (vs.capitate),tricolporatepollenporate,though all speciesinsects. and Africa. At least30speciesof and southeast Asia, aswellmanyspeciesfrom the Americas for support.Thisgroup includes allspeciesinMadagascar Vahihara, cies of that differ indetailsoftheirgrowth formsfrom shrubby spe- neotropical sect. likely exhibitssubstantialvariation.Speciesoftheexclusively tional studiesof refer totheseplantsassemi-self-supporting, althoughfunc- tional studiesofclimbingplants (Speck andRowe1999) and over nearbyvegetation.We adopttheterminologyoffunc- in pricklesormore rarely spinesthatare usedtoscramble of development,oftenwithlongcurvingbranchescovered shrubs thatmaybeleaningorsemi-scandentatsomestages there are fewexamplesoffamiliesthat includebothclimbing evolved many timesindependently. Despitethisdiversity, have ledtothehypothesisthat climbinggrowth forms have tions havechangedsincethis publication);suchobservations plant families( Gentry 1991 , althoughfamilycircumscrip- cally widespread, inoneestimateoccurring133vascular forms, particularlyoflianas. Climbing plantsare taxonomi- opportunity totesthypotheses ontheevolutionofgrowth 1990 ). and twoinsect. described assmall,erect trees, toca.8m,twoinsect. of South America. Onlyfourspeciesof seasonally floodedrivers,andinotheropenwetareas with thislastgrowth formoccurinthellanos,cerrado,along erect, withrigidlinear, lanceolate,orsagittateleaves.Plants most branchingoccurringclosetoground level;branchesare hemicryptophytes, orchamaephytes( Cristóbal 1976 ) with The diversityofgrowth formsin The variation foundamongthesespeciespresents an Byttneria Ayenia Byttneria Rayleya, are lacking. Although Cristóbal (1960 , 1976 ) didnot are unarmedlianasthatrely onotherwoodyplants Ayenia, Ayenia showremarkably more variationingrowth form. are trithecate,asin are Ayenia, Byttneria, andallcloseoutgroups ( Whitlock etal.2001 ), and Crassipetala Byttneria Byttneria haslongbeenappreciated. However, asis havebeendescribedassmalltrees (fourto < 1mtalland,inespeciallydryregions, may Urticifolia Ayenia are lacking,andthisgroup ofplants consistoferect shrubs orsubshrubs . Theseplantsmaybegeophytes, ( Cristóbal 1976 ; Barnett andDorr , , Byttneria Ayenia and Crassipetala Byttneria Byttneria Rayleya . Thegenusdiffers from Ayenia , allmembersofsect. Byttneria (manythoughnot , and initsdecurrent and , andtoalesser Incasica Byttneria havebeen Ayenia Vahihara and ) are ) , as ,

in thefuture. candidates forcomparativestudiesoffunctionalmorphology logenetic frameworkthatcanbeusedtoidentifyappropriate two independentradiations. A finalgoalistoprovide aphy- sect. clade; and(4)speciesof (3) neotropical speciesofboth between self-supportingplantsandfullyscandentlianas; and shrubs represent aphylogeneticallyintermediateform supporting, erect growth form;(2)semi-scandenttrees there are noreversals from alianescentgrowth formtoaself- evolution ofgrowth forms andbiogeography, including(1) Ayenia corroborate reports intheliterature ofgrowth formsfoundin tion, wesurveyrecently collectedherbariumspecimensto evolution ofcharactersusedtodelimitbothgenera.Inaddi- nomic samplingofbothgenera,andanexaminationthe of themonophyly their geographicranges.Ourfirstgoalsare additionaltests cal diversityinbothgeneraandsamplingfrom throughout Rayleyabahiensis, species of from ninespeciesof for thisgenus. sections, Cristóbal (1976) hypothesizedaneotropical origin Byttneria ical andtaxonomicdiversity. Because60%ofthespeciesin that currently occurthere, aswellthegreater morpholog- nated intheformerbecauseofgreater numberofspecies Ayenia and EasternBrazil,with10endemicspeciesallinsection three sectionsthatsherecognized; and(2)Bolivia, Paraguay, Antilles, withatleast38endemicspeciesdistributedinall sity in ronments. Cristóbal (1960) recognized twocentersofdiver- of Argentina andUruguay. Within this range,however, species typic representatives from fourofsixsections( Cristóbal 1976 ), plusthemono- resentatives ofninespecies closely related Byttnerieae( from five otherByttnerioideaeasoutgroups (Appendix1),including two as wellaSouth American collection.Inaddition, weusedsequences across thetropics, DNA from thefewherbarium specimens availableof sections recognized by Cristóbal (1960) , 27specimensof without success.Foronespeciesof the southernU.S. A. ( tributions, atleastabroad geographicscale,extendingfrom shrubs. ate formbetweenlianasandfullyself-supportingtrees and such semi-self-supportingplantsrepresent an intermedi- vide anadditionalphylogenetictestforthehypothesisthat the manyleaningandscramblingspeciesof and shrubs aswell60+speciesoftrue lianas.Inaddition, a reversal, becauseitincludesseveralspeciesoferect trees Byttneria/Rayleya is inferred tobebasal( Rowe andSpeck2005 ). The and self-supportinggrowth formsinwhichtheclimbinghabit Here, weanalyzesequencesfrom three chloroplast regions Within the Americas, Ayenia aooi Sampling— Taxonomic Rayleya bahiensis Byttneria and subsect. Ayenia are American withrepresentatives offivethesix tendtobemore limitedtodrier habitats,whereas Byttneria Byttneria : (1)northernCentral America, Mexico,andthe ) occurringinseasonalopenhabitatsrepresent B. catalpifolia Ayenia cladeisapromising group tosearch forsuch withgoodrepresentation ofmorphologi- aeil ad Methods and Materials (Appendix 1).We madeseveralattemptstoextract canbefoundinbothdryandmesicenvi- . We thentestspecifichypothesesonthe Ayenia Ayenia We sequencedchloroplast markersfrom rep- . Shehypothesizedthat Ayenia Ayenia Abroma Ayenia , weincludedaCentral African collection Ayenia ) orSonora,Mexico( and , 27speciesof Byttneria and and withrepresentatives from all three Ayenia and Byttneria Byttneria Kleinhovia withadisjunctdistribution Byttneria and withgreater taxo- ), twoLasiopetaleae have similar dis- Byttneria Byttneria, (i.e. Megatritheca, Byttneria Ayenia Byttneria Byttneria Byttneria form a Ayenia/ origi- pro- and with ) to ), but

Copyright (c) American Society for Plant Taxonomists. All rights reserved. Delivered by Ingenta to IP: 192.168.39.211 on: Sun, 03 Oct 2021 00:44:52 Maddison and2005 ). most parsimonioustree usingparsimony(implementedinMacClade 4.08; tropics; and(4)Madagascar. All characterswere optimizedonthepoolof with thefollowingstates:(1)NewWorld; (2) Asian tropics; (3) African A secondcharacterdescribinggeographic descriptionwasestablished shrubs, andsubshrubs; (2)semi-scandenttrees and shrubs; and (3)lianas. scored thatappeartocorrespond tothevariationobserved:(1)erect trees, A), anddatafrom herbarium specimenlabels.Three characterstateswere recently collectedherbarium specimens(primarilyfrom MO,NY, GH,and from previously publishedreports, supplementedbyobservationsfrom 0.01 whichwere obtained after8.9x10 standard deviationofsplitfrequencies betweenthe tworuns of lessthan 0.2) toimprove mixing.Convergence ofruns wasindicated by average 100 generations.Three ofthefourchainswere heated (sequentialheat= parsimony-informative characters,respectively, and 0.8%of from the 131 HALE: AYENIA, WHITLOCKAND BYTTNERIARAYLEYA AND two setsofPCRprimers:the3 method ( Kim etal.1997 ). We sequencedthree chloroplast markersusing using DNeasycolumns(QiagenInc.,Valencia, California)ora6%PVP material thatwassilica-gel-dried,air-dried, orfrom herbariumspecimens results of Whitlock etal.(2001) . ( 2011] growth formsof rule consensustree andtocalculateposterior probabilities (PP). by-generation plot.Theremaining trees were usedtoproduce amajority- were discarded asburn-inaftervisualexaminationofthelikelihood- cent Unambiguously alignedinsertionsanddeletions(indels) analyzed withbothmaximumparsimonyandBayesiananalyses. HM488369-HM488452). et al.1985 ). All sequencesare availableinGenBank(accessionnumbers identified bycomparisontopublishedsequencesof Corp., Ann Arbor, Michigan).Theboundariesofadjacentregions were and stopcodonsincodingregions usingSequencher3.0(GeneCodes DNA analyzer. Sequenceswere assembledandinspectedforframeshifts ing protocols. Sequencingreactions were run onan ABI 377or3730xl in bothdirections using ABI BigDyedye-terminatorsandcycle-sequenc- standard exo-SAP procedure. Double-strandedproducts were sequenced internal primerswere excludedfrom allanalyses. primers c/dande/f( Taberlet etal.1991 ). The21sitesrepresenting the DNA, internalPCRprimerswere usedtoamplifytwosmallerfragments: ers candf( Taberlet etal.1991 ). Inafewcasesofspecimenswithdegraded and product wassequenceddirectly withthePCRprimers.The matK9R ( Manos andSteele1997 ) thatamplifieda930bpproduct. This each withfourlinkedchainsfor1 used amongpartitions.We conductedtwosimultaneousMCMCruns and were unlinkedamongthefourpartitions. A variableratepriorwas indels. Modelparameterswere derivedfrom default priordistributions ters, estimatedfrom thedata. A binarymodelwasappliedto14coded alpha estimatedfrom thedata)andI,proportion ofinvariantcharac- with agammadistribution(fourratecategoriesandtheshapeparameter when appropriate. Across siterateheterogeneity wasthenincorporated cal nucleotidefrequencies andrateparametersestimatedfrom thedata and models (JC,F81,HKY, GTR)foreachofthethree datasets( Crandall 1997 ) wasusedinitiallytotestthefitoffourevolutionary and Huelsenbeck2003 ). Thelikelihoodratiotest( Huelsenbeck and bootstrap replicates, eachwith100randomadditionsequencesearches. replicates. Bootstrapsupport(BS; Felsenstein 1985 ) wasestimatedwith100 2002 ) usingheuristicsearches withTBRand100randomadditionsequence A combinedalignmentisavailableinTreeBASE (studynumberS10616). a concatenateddatasetcombining sequences usedwere from thechloroplast, allanalyseswere performedon coded asbinarycharactersandincludedinallsearches. Becauseallthe Guichenotia The alignedmatrixincludes938bpfrom Mlclr Methods— Molecular Biogeography andGrowth FormEvolution— Pyoeei Analyses— Phylogenetic PCR products were cleanedwithQIAquickcolumns(QiagenInc.)ora Bayesian analyseswere implementedwithMrBayes3.1.2( Ronquist The parsimony analysiswasperformedwithPAUP* 4.0b10( Swofford trnL-trnF trnL-trnF trnL-trnF and trnL-trnF spacerusuallyamplifiedinasingle1.2kbpieceusingprim- ), usingoneofthemostparsimonioustrees, withempiri- spacer. Forthe Rulingia Ayenia region with103(11%) and124(10%) , , ) andoneTheobromeae ( Byttneria, Rayleya Total genomicDNA wasextractedfrom leaf All sequenceswere alignedbyeyeand matK ′ endof Results matK × region, weusedprimersmatK4Fand 10 6 matK generations,samplingtrees every , the 5 generations.Thefirst2,500trees andoutgroups wasobtained , the trnL intron, and trnL Theobroma matK nomto o the on Information intron andtheadja- Nicotiana and1,224bp > trnL-F onebpwere ) following ), matK, trnL, trnL (Sugita spacer. intron

sect. sect. Crassipetala neotropical cladeincludes theremaining speciesofsect. cal representatives ofsect. morii representatives ofsect. 100). Relationshipsamongthesetaxaandotherneotropical a conspecificspecimencollectedfrom Peru (BS=100,PP = representative from tropical Africa inthisstudy, issisterto ported clades.(1) All speciessampledof although wecannotreject thispossibility. the twoothermembersofsectionthatwere sampled, genus. Ouranalysesdonotshowthatitformsacladewith This lastneotropical clade issisterto sects. scrambling shrubs. Specimensof in particulardistinguishinglianasfrom semi-scandentor confirm Cristóbal’s (1960 , 1976 ) descriptionsoftheseplants, low (BS=51,PP simony consensus;however, supportforthisrelationship is identical sequences.Onespecimenof but lowbootstrapsupport(BS=51)despitecontainingnearly form asubcladethathashighposteriorprobability (PP =94) supported (BS=93,PP = 100); thefour Asian specimensalso the fiveMalagasyspecimensformasubcladethatiswell- Vahihara tative ofsect. a paraphyleticsect. sampled from sect. neotropical (BS =100,PP =100)andnestedwithinacladeofexclusively ndhF support isnotstrong (BS=62,PP =58). As wasfoundinthe all sampledrepresentatives of well-supported clade(BS=100,PP =100). analyses, all consensus revealed bytheBayesiananalysis( Fig. 1 ). Inboth of theparsimonyanalysiswasidenticaltomajority-rule steps (C.I.=0.81,R.0.91; Fig. 1 ). Thestrictconsensus ing 15indelsresulted in243equallyparsimonioustrees of569 for eachpartitionofthesequencedata. 2–145bp inlength.LikelihoodratiotestsselectedGTR+gamma 9bp were codedfrom matrix cellsscored asmissingdata.Two indelsof6bpand from sects. agreeing wellwith Cristóbal’s (1976 ) descriptions.Specimens almost alwaysdescribedaslianas,oftenintrees is inferred to beanerect tree or shrub. Within thecombined mon ancestorof thecombined were similaracross all 243mostparsimonioustrees. Thecom- the characterstate“semi-scandent trees andshrubs.” The growth formofthesespecieswere therefore codedwith these plantstoclimbandscramble overnearbyvegetation. nificantly inthepresence ofpricklesandspinesthat enable plants alsodiffer from thelianasofsect. tative morphologyandarchitecture ofthesesemi-scandent ing shrubs, againagreeing with Cristóbal (1976) . Thevege- always describedasleaning,scandent,scramblingorclimb- All specimensof Observations from recently collectedherbariumspecimens Unweighted parsimonyanalysisofthe42sequencesinclud- All reconstructions ofthecharacterdescribinggrowth forms analysis( Whitlock etal.2001 ), and Byttneria Byttneria Crassipetala are aclade(BS=100,PP =100).Within thisclade, B. schunkeii sampled, all representatives ofsect. Crassipetala Byttneria Byttneria sampled(BS=100,PP =100).Ofthese,only ismonophyletic(BS=100,PP =100), while Ayenia < and 50). Leiayenia Cybiostigma Byttneria . Within , , (BS=100,PP =100)are bothneotropi- , , matK A. praeclara, and Urticifolia Ayenia, Vahihara Crassipetala and13from the formacladethatisnestedwithin Urticifolia sampledformthree well-sup- Ayenia and Ayenia . Thepositionofonerepresen- Ayenia/Byttneria/Rayleya are unresolved. (2) bothappearpolyphyletic. Byttneria isunresolved withinthe , thetworepresentatives Rayleya and , incontrast,are almost Ayenia . (3) A large exclusively Ayenia B. catalpifolia Vahihara Byttneria sect. Rayleya togetherforma ismonophyletic inthestrictpar- trnL/trnF Byttneria Urticifolia Vahihara > issisterto , mostsig- , although , 10mtall, , theonly Byttneria region, clade sect. and are Copyright (c) American Society for Plant Taxonomists. All rights reserved. Delivered by Ingenta to IP: 192.168.39.211 on: Sun, 03 Oct 2021 00:44:52 Bayesian majority-rule consensusshowparsimony bootstrapvalues/Bayesianposteriorprobabilities ( [Volume 36 SYSTEMATIC BOTANY 132 on thetree. Sectionsof gin. Theplesiomorphic growth formforthe however, allclose outgroups tothecombined are below. Shadingofbranchesindicatesinferred geographicdistribution. Reconstructions ofgeographicdistributioninthemo Fig 1 . . Pyoey f of Phylogeny Byttneria Ayenia, Byttneria, following Cristóbal (1976) are onthefar right. and Ayenia/Byttneria/Rayleya Ayenia/Byttneria/Rayleya Rayleya . Oneof243mostparsimonioustrees. Nodesappearingintheparsimonystrict consensusand cladeisinferred as self-supportingtrees and shrubs; inferred transitionsare indicated cladeare paleotropical. Growth formsofincludedtaxaare shownontherightmar- × 100) abovebranches;parsimonybranch lengths st basalnodesisuncertain; Copyright (c) American Society for Plant Taxonomists. All rights reserved. Delivered by Ingenta to IP: 192.168.39.211 on: Sun, 03 Oct 2021 00:44:52 Ayenia 133 that havebeenusedtocircumscribe generaandsectionswith gests complexpatternsofevolutionthefloralcharacters inferred tobeneotropical. The commonancestorofthe erect shrubs andsubshrubs foundin of semi-scandenttrees andshrubs, there isareversal tothe HALE: AYENIA, WHITLOCKAND BYTTNERIARAYLEYA AND independently from lianasofsect. growth formwithintheneotropics thatappearstohave arisen ond transitionfrom erect trees andshrubs toasemi-scandent dence ofreversals toerect trees andshrubs. There isasec- includes allspeciesof lianescent growth forminthebranchleadingtocladethat Ayenia/Byttneria/Rayleya 2011] ( dithecate stamens,whereas allbasallineagesoftheingroup teen ( of plants. All potentialoutgroups inourstudyhaveeitherfif- tional homoplasyinstamennumberwithinonesmallclade of stamennumberasacharacter. Ourresults suggestaddi- Whitlock etal.2001 ), raisingquestions ontheusefulness these taxaare nonmonophyletic (e.g. Alverson etal.1999 ; Molecular phylogeneticanalyseshaveshownthatmanyof ing membersofthe“” (e.g. Hutchinson 1967 ). sized indelimitingfamiliesandgeneraofMalvales,includ- androecium, particularly stamennumber, hasbeenempha- reveal more complicatedhistoriesoftheseplants. Ayenia also needstoberevisited in lightofourphylogeneticresults. phores, bothfoundin mens in (from fivetoten,with dithecateandfiveunithecatesta- number (from tentofifteen) oradoublingofstamennumber eage thatcanbeinterpreted alternatelyasanincrease intheca cates asecondaryproliferation oftheandroecium inthislin- Rayleya eage leadingtothecommonancestorof thus evidenceforareduction instamennumberthelin- ever, anandrogynophore isalsopresent in petal clawsappeartobeunique dently derivedinthesetwolineages.Thealmostthread-like clade ( Fig. 1 ), suggestingthatbothcharactersare indepen- cies of Leinfellner (1960) examinedpetaldevelopmentinfivespe- these complexthree dimensionalstructures. Forexample, patterns ofpetalevolutionandtoidentifyhomology in clade ( Whitlock etal.2001 ). ably thenearest sistergroup tothe projections thataffect thecomplexthree-dimensional fitofthe one anotheracross species,withvarious grooves, ridges,and The formofbothstructures variessubtlyandinconcertwith characters usedtodelimitsections in these structures meet.Suchanapproach hasprovided many ogy ofthepetalsandstaminal columnattheirapiceswhere A similarapproach maybeneededtointerpret themorphol- identified commonalitiesat early stagesacross these taxa. Rayleya The findingthat Implications forFloralEvolution— The homologyofconstrictedpetalclawsandandrogyno- Floral developmentalstudiesmayhelptoilluminate Kleinhovia, Abroma, Scaphopetalum and and Ayenia, . Thepositionof and Ayenia Rayleya Byttneria Byttneria six ). Byttneria are notcloselyrelated inthecontextofthis Ayenia . Additional samplingispredicted to ) have fivedithecatestamens.There is Ayenia Byttneria clade,there isonetransitiontoa Discussion Ayenia , and13otherByttnerioideae, and isnestedwithin and Ayenia, Byttneria, insect. nestedwithin Rayleya Vahihara Ayenia Ayenia/Byttneria/Rayleya Byttneria Vahihara Ayenia ) orten( Ayenia, Byttneria, opooy f the of Morphology butnotin and . Within thisgroup Kleinhovia and sect. and Byttneria Byttneria Rayleya , withnoevi- Leptonychia Rayleya Byttneria Byttneria Byttneria , prob- , ; how- ; indi- sug- and is ) . , .

ingroup sampledhere, ( Cristóbal 1976 ). Thelineagesistertotheremainder ofthe occurring inopen,seasonallydryand/orfloodedhabitats are erect, oftenrhizomatous shrubs orsubshrubs mostly group ofover20species,allnativetoSouth America that relatives. Section of the unusualarchitectures, leafmorphologies,andecology tional transitionsbetweenthesegrowth forms.Nevertheless, likely includesomeuprightshrubs, thusthere maybeaddi- growth form.However, thetaxathatwescore assemi-scandent umented exampleofareversal from asemi-self-supporting and subshrubs of this growth form. taxonomic distributionorfrequency, ortransitionstofrom distinguished from lianas orvines,littleisknownabouttheir et al.2005 ). Becausesemi-self-supportingplantsare rarely pendent transitionsfrom lianas toashrub-like habit( Lahaye group of Apocynaceae, forexample,there have beenfiveinde- forms withinasinglecladeofcloselyrelated species.Inone tiple reversals from climbingformstoself-supportinggrowth In someexceptionalexamples,however, there maybemul- stantial numbersofbothclimbingandnonclimbingspecies. sampled phylogeneticanalysesofgroups thatincludesub- such observationsislimitedbythesmallnumberofwell- the climbinghabitispresumably derived).Thegeneralityof erwise madeupalmostentirely oftrees andshrubs (andthus Convolvulaceae), manyclimbersare infamiliesthatare oth- while somefamiliesconsistalmostentirely ofclimbers(e.g. taxonomic distributionofclimbingspecieswhonotesthat, This isconsistentwith Gentry’s (1991) observationsofthe condition isalmostalwaysinferred tobeself-supporting. both climbingandself-supportingplants,theplesiomorphic et al.(2003) statethatinmostexamplesofcladesinclude from semi-self-supportingplants,apartfrom thisstudy. Speck lianas toself-supportinggrowth formsandperhaps none to lianas sampledformawell-supportedclade,corresponding trees andshrubs, ortoanyothergrowth form. All speciesof found noevidenceofareversal from lianastoself-supporting eage ofsemi-self-supporting,scramblingshrubs ( Fig. 1 ). We gave risetoalineageoflianasandsecondindependentlin- self-supporting commonancestorof of sect. in thebranchleadingto primarily semi-scandentplantstoerect shrubs andsubshrubs However, ourresults showareversal from whatappeartobe any othergrowth formorfrom anyothersection ( Fig. 1 ). such as similar towhatisseeninclosely related semi-scandentshrubs broad, palmately-veined,toothedleaves,andprickly stems pled species generally occurs atorclosetoground level, withplantsdying ceolate, tosagittate, alluncommoninMalvaceae. Branching secondary venation,andleaf shapes rangingfrom linear, lan- and entire, coriaceousleaveswithprominent, oftenparallel terns ofevolution. this complexmorphologymayhaveequallycomplicatedpat- two sectionsineachgenus(Appendix1; Fig. 1 ) suggeststhat petals tothestaminalcolumn.Thenonmonophylyofatleast The transitionfrom semi-scandentplantstotheerect shrubs There are fewdocumentedexamplesofreversals from Eouin f rwh Forms— Growth of Evolution Byttneria Byttneria B. urticifolia Byttneria sect. sect. B. dentata are generallyshorter, haveunarmed stems Vahihara Byttneria Byttneria Byttneria and ), isanerect shrub, 2.5mtall,with Byttneria scabra Byttneria B. divaricata , thatdoesnotincludeplantswith sect. markadivergence from itsclose isamorphologicallycohesive Byttneria sect. Our results suggestthata ( Fig. 1 ). All otherspecies Byttneria (aswellasanunsam- Ayenia maybethefirst and (Fg 1). (Fig. Byttneria doc-

Copyright (c) American Society for Plant Taxonomists. All rights reserved. Delivered by Ingenta to IP: 192.168.39.211 on: Sun, 03 Oct 2021 00:44:52 3 SSEAI OAY [Volume 36 SYSTEMATIC BOTANY occurs in similar adaptations. A secondinvasionofdry, openhabitats shrubs andsubshrubs of tion andfewerhostsforlianas.Theremarkably monocot-like that grow inopendryhabitatswere duetoreduced competi- that transitionstomore shrub-like habitsin Apocynaceae open andseasonalhabitats. Lahaye etal.(2005) speculated ification inleafmorphologyassociatedwithinvasionofmore ing growth formpreceded areduction instature andthemod- of sect. a fewspeciesof nectaries (vs.multiaperturateinotherspeciesof fire. All speciesare alsounitedinhavinguniaperturatefoliar back totheground inadverseconditionssuchasdrought or 134 a relatively basallineagewithinthe of Kleinhovia branching. Bothoftheclosest outgroups, subsequent trends towards reduced stature and/orincreased suggest thecommonancestorofthiscladewasatree, with trunk. Although oursamplingisnotcomplete,results a tree, oranuprightwoodyplantwithasingle,well-defined Byttneria the independentlyderivedsubshrubs of growth forms,andself-supportingspeciesof with speciesof and semi-scandentshrubs, semi-scandentspeciesof with differing growth forms,inparticulartocompare lianas similarities anddifferences betweencloselyrelated species tem withwhichtoexplore anatomicalandarchitectural The current phylogeny, however, provides apowerfulsys- never beeninvestigatedinanyspeciesof constraints (ifany)thanlianas. forms mayfacedifferent developmentalandphysiological the case,thentransitionsfrom semi-self-supportinggrowth rounding vegetationand interlockthebranches.Ifthisis in mature lianashoots,and insteadmaysimplyleanonsur- cal properties seeninlianas orthestructural noveltiesfound plants maynotexhibitdevelopmentalchangesinmechani- Rowe andSpeck(2004) suggestthatsemi-self-supporting supporting plantsasaclasstendtohavecambialvariants. eral lackofinformationaboutthem.Itisnotclearifsemi-self- ideas tosemi-self-supportingplantsislimitedagainbyagen- supporting forms( Speck etal.2003 ). Application ofthese provide amechanismby which lianascouldevolveintoself- ing species,asimpleretention ofjuvenilecharacteristicsmay with anatomysimilartowhatisseeninmature self-support- often haveaself-supportingstageasseedlingsorreiterations, forms ( Rowe andSpeck2004 ). Alternatively, becauselianas against transitionsfrom lianastoself-supportinggrowth lianas mayposedevelopmentorecologicalconstraints open habitats. innovations inanindependentinvasionofdry, seasonal,and suggesting that species are lowwithprocumbent ordecumbent branches, are uprightself-supportingplants,althoughmanyother Guyana. B.schunkei from three ofthesetree species, The result that Perhaps themostuncommongrowth forminthiscladeis To ourknowledge,the anatomyofsecondarygrowth has The cambialvariantsinsecondarygrowth seeninmany Ayenia Byttneria . Byttneria morii andfourof , are smalltrees. Itappearsthatonlytwospecies Ayenia from thePeruvian Amazon, and suggeststhatthetransitiontoaself-support- Ayenia . All speciesof Ayenia Byttneria scabra Ayenia Byttneria ). and underwentdifferent morphological withprocumbent anddecumbent Byttneria B. schunkei are arborescent. We sampled Ayenia issistertoallothermembers B. morii sect. Ayenia/Byttneria/Rayleya sampledinthisstudy appeartobetogether from French Guiana, Byttneria Ayenia A. praeclarae Byttneria Byttneria Abroma or Ayenia mayreflect Byttneria Byttneria sect. with from and and .

( Cristóbal etal.1992 ). Theotherspeciesof ries andishypothesizedtobecloselyrelated to been describedastrees, biogeographic patterns(seebelow). Rayleya will showtheselineagesnearthebaseof expect thatfuture analysesthatincludethese African taxa form isindeedanindicatorofphylogeneticrelationships, we sect. east Africa, are alsounarmedandhavebeenbothplacedin Byttneria presence offoliarnectaries,atraitfoundinallsections a basalpositionwithinthe rescent speciesof Arbo 1971 ; Cristóbal etal.1992 ; Dorr 1996 ). Theotherarbo- Byttneria Rayleya in ouranalyses. lineages withinthecladethatare notstrongly supported conclusion, however, dependsonrelationships amongbasal prediction basedonthe diversitywithin tropical aswell( Fig. 1 ), consistent with gesting thatthecommonancestoroftheseplantswasneo- Cristóbal’s (1976) Byttneria/Rayleya to thesetwospecimens ( Fig. 1 ). folia cific specimenfrom Peru. Theuncertainpositionof B.catalpifolia belongs tothemostwidelydistributed speciesinthegenus, The onespecimenfrom Africa thatwewere abletosample lineages withinthelianaclade are poorlysupported( Fig. 1 ). taxa are undersampledhere andbecauserelationships among African andMalagasylineagesof cannot rule outthepossibilityofacloserelationship between Africa, mostlikelytheresult ofrecent Cenozoicdispersal.We ter group relationship betweenlineagesfrom Madagascarand Nowak (2006) foundthatthemostcommonpatternwasasis- of thebiogeographicoriginsMalagasybiota, Yoder and neotropical lineageinallreconstructions. Inarecent review diversity islow. keys tospeciesfortheregion, anditispossiblethatspecies many namesexistfor Asian taxa,there are nocomprehensive Asia appearstobelessdiversemorphologically. Although and dramaticheterophylly. Incontrast, 27 speciesoflianas,manywithunusualleafmorphologies Byttneria may represent athird paleotropical radiation.InMadagascar, men thatwewere ableto samplefrom Africa, otropics, inMadagascarand Southeast Asia. Thesolespeci- appear tobeatleasttwoindependentradiationsinthepale- lineages withinthelianacladeare notfullyresolved, there and are twosmall Australasian genera, et al.2001 ). Although theclosestoutgroups ofthisclade era ofByttnerieaeare exclusively paleotropical ( Whitlock morphologically andinthenumberofspecies. All othergen- apparently paraphyletic Rayleya in Byttnerieaethatmanyspeciesoccurthe Americas. clade. Relationshipsof Biogeography— All paleotropical taxasampled withinthe Unexpectedly, theMalagasycladeof maybeduetotheextraordinarily longbranchleading up Abroma Vahihara, clade,althoughthismayresult inmore complicated cladeare derivedfrom withinthecladeoflianas,i.e. and butlimitedtosevenspeciesin sect. displaysaremarkable radiationofapproximately (1–2species),thebasallineagesof andformsa well-supportedcladewithaconspe- Ayenia Vahihara onthebasisoffloralmorphology. Ifgrowth cladeare predominantly neotropical, sug- h The Ayenia onlyoccurinthenewworld,and ( Fig. 1 ). Although relationships among Ayenia/Byttneria/Rayleya A. praeclarae Byttneria B. fruticosa , , A. stipularis, Ayenia ismostdiversethere, both cladeissupportedbythe are unresolved; however, Byttneria and Kleinhovia alsohasfoliarnecta- Ayenia, Byttneria Byttneria B. glabra Byttneria bcue African because Ayenia/Byttneria/ Ayenia/Byttneria/ cladeisunusual Byttneria (Citbl and (Cristóbal (monotypic) B. catalpifolia inSoutheast issistertoa A. praeclarae , bothfrom thathave B. catalpi- Ayenia/ . This . ,

Copyright (c) American Society for Plant Taxonomists. All rights reserved. Delivered by Ingenta to IP: 192.168.39.211 on: Sun, 03 Oct 2021 00:44:52 Byttneria Tuamotu inFrench Polynesia. is foundfrom MexicotoBolivia,withdisjunctpopulations in uted speciesnotsampledhere, Atlantic ( Thorne 1973 ; Renner 2004 ). A secondwidelydistrib- additional exampleofarecent disjunctionacross thetropical of thedirectionality ofdispersal, gin, withsubsequentdispersaltotheneotropics. Regardless and ofother African speciesmayyetreveal an African ori- neotropics to Africa, additionalsamplingwithinthisspecies gest thatdispersalwithin the parsimonyoptimizationsofgeographicdistributionsug- cal sequences( Fig. 1 ), supports thisspeciesconcept. Although mens thatwesampledare closelyrelated withnearlyidenti- ( Cristóbal 1976 ). Our findingthattwowidelyseparatedspeci- Mexico to Argentina, aswellintropical Africa, andTahiti catalpifolia, recently, betweentheneotropics andpaleotropics. favor ofatleastsomelongdistancedispersalevents,probably the widedistributionofafewspecies able toByttnerioideaeare mostlyofrecent origin.However, fossils of substantial rateheterogeneity ( Fig. 1 ). There are noknown lenging becauseofalacksuitablecalibrationsaswell divergence timesinthe neotropics andpaleotropics isofgreat interest, assigning described assarmentose,orcreeping. One speciesisdescribedasashrub, whereas theotheris phology orgrowth form ofthetwospecies appendages ( Cristóbal 1965 , 1976 ). Littleisknown of themor- such asthebroad petal claws andprominent fleshypetal are consistentwiththeparaphyletic paleotropical lineage.Other aspectsofitsfloralmorphology trithecate antherssuggest,itwouldrepresent anadditional to theexclusively American speciesof ography withinthisgroup. If our understandingofmorphologicalevolutionandbioge- Megatritheca lianas toself-supportingtrees. African ics. Alternatively, ifthesetwospeciesare closelyrelated tothe Vahihara of thecladeorperhaps sistertotheremaining taxa ofsect. Byttneria arborescent growth formisplesiomorphicwithinthe differ inthatbothare small,unarmedandupright trees. Ifan Vahihara floral morphologyofthetwoEast African speciesinsect. to neotropical lineageswithsimilarmorphology. Whilethe dent radiationinthe African tropics iftheyare closelyrelated spiny, scramblingshrubs andmayrepresent anindepen- cies ofthenonmonophyleticsect. from Central Africa ( Cristóbal 1965 , 1976 Africa, andtwospeciesinthesegregate genus ). The African spe- poorly collectedspeciesinsect. species of 01 WILC N AE YNA YTEI N ALY 135 HALE: AYENIA, WHITLOCKAND BYTTNERIARAYLEYA AND in growth forms.Inadditionto terns ofbiogeography, andtofurtherexamplesoftransitions pling of African taxawilllikelyleadtomore complicatedpat- 2011] Long distancedispersal issomewhatunexpectedin Although thetimingofshiftsindistributionbetween The unsampledand rarely collectedcentral African genus Atog Although B. catalpifolia , representing anadditionallineageinthepaleotrop- isconsistentwithothermembersofthesection,they given itsfruit morphology. clade,thesetwotaxashoulddiverge atthebase Byttneria, Ayenia, forexample,occursintheneotropics, from Byttneria promises toprovide additionalcomplicationsto Byttneria insect. , theymayrepresent areversal from true isnotdiversein Africa, additionalsam- Ayenia/Byttneria/Rayleya or B. catalpifolia Vahihara Megatritheca B. aculeata Rayleya, Crassipetala B. catalpifolia B. catalpifolia Byttneria Crassipetala from East Africa, three Byttneria andthefewassign- Ayenia occurred from the ofsect. Byttneria iscloselyrelated endemictoWest sect. , asitsunusual , there are two fruits are five- appeartobe cladeischal- provides an Megatritheca Megatritheca Crassipetala Crassipetala argues in Byttneria Ayenia/ , . ,

to tropical rainforests. Informationonthehabitatoccurrences Rayleya persal event. may alsofacilitateestablishmentinnewareas afterarare dis- general abilityformanylianastothriveindisturbedhabitats cies mayreflect inpartitsweedyhabit( Cristóbal 1976 ). The and Central America andthewidedistributionofthisspe- Byttneriaaculeata at leastsome ther hasbeenreported. Oncedispersed,theweedynature of to thefeathersorfurofbirds andmammals,althoughnei- conceivable thatsomefruit maybedispersedbyattachment most ofteninvokedinlongdistancedispersal.However, itis for dispersalbyendozoochory, wind,orwater, theprocesses armed withhooksorspines.There isnoobviousadaptation from 0.5–4cmindiameter. Theyare dryandwoody, often seeded capsulesorfiveone-seededmericarps,ranginginsize sect. sonal savannahsofSouth America occurswithin and theCaribbean. A secondindependentradiationintosea- in desertsandscrublands inMexico,thesouthernU.S. A., sent twoindependentlineages.Manyspeciesof grow inopenhabitatswith pronounced dryseasonsrepre- However, ourphylogeneticresults suggestthatplants for mostspeciesisincompleteandthusdifficult toquantify. Avro, . . B A Wilc , . yflr C Byr ad . . Baum . A. D. and Bayer , C. Nyffeler , R. Whitlock, A. B. S., W. Alverson, to D. A. Baum). Harvard University, andtheNationalScience Foundation(DEB9876070 tively. Thiswork wassupportedbyfundsfrom theUniversityofMiami, collecting Marshall Hedin,Mahera Anjum, andMartinCheekprovided assistancein Libraries atHarvard University forhelpwithliterature. JenniferTalbot, to samplefrom herbarium specimens,andthelibrariansofBotany Garden (MO),andthe University of Arizona (ARIZ)forpermission (A andGH),theNew York BotanicGarden (NY),theMissouriBotanical tions inthe within aregion? We are justbeginningtoaddress suchques- Are plantswithsomegrowth formsmore likelytodiversify forms more likelytodisperse toandestablishinnewregions? viously uninhabitableregion? Are plantswith somegrowth Do changesingrowth form allowalineagetoinvadepre- forms contributetodiversityatmultiplegeographicscales. an opportunitytoexaminehowplantswithdiffering growth growth formsassociatedwith more seasonalconditions. open habitatsofSouth America in that achangeingrowth form preceded invasionofseasonal, scale patternsoftropical plantdiversity. shed lightontheevolutionaryprocesses thatunderlielarge- may allowustoaddanewdimensionfloristicstudiesand with comparativeanatomicalanddevelopmentalstudies, as Madagascar. Expandedsamplingofspecies, combined some regions showingaremarkable radiationoflianas,such growth formmayhave an increased speciationrate,with the majorityofspeciesdiversity, suggestingthatthis Within the establishing andradiatingintonewcontinentallandmasses. a broader geographicscale, lianasappearmore successfulat Within theneotropics, membersofthe Acknowledgements. Phylogenetic analysesofcloselyrelated speciesprovide aa. data . 1999 . Phylogeny of thecore :evidence from Byttneria cladeare foundinawiderangeofhabitats,from deserts Ayenia American Journalof Botany Ayenia/Byttneria/Rayleya Ayenia/Byttneria/Rayleya . Inbothlineages,plantshaveevolveddifferent and Byttneria , forexample,isaseriousweedinMexico Byttneria We thanktheHarvard UniversityHerbaria ieaue Cited Literature speciesmayfacilitateestablishment. in Arizona, Florida,andCameroon, respec- 6 1474–1486. 86: Byttneria clade,lianasaccountfor clade.Our results show sect. Ayenia/Byttneria/ Ayenia Byttneria ndhF Byttneria sequence occur . At .

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Hispaniola; HM488386,HM488428; HM488385, HM488427; and Whitlock1912 Schunke4567 23755 (GH); Brazil;HM488378,HM488420; Australia; HM488408,HM488450; Mart. exK.Schum.; Cristóbal; Widely distributedinSouth America; HM488383,HM488425; HM488424. HM488423; B.stenophylla 10272 (FTG); Australasia; HM488407,HM488449. Australasia; HM488406,HM488448; Cantino691 Southwestern U.S. A.; HM488369,HM488411; 1981 , and1985 ), Barnett andDorr(1990) Geographic distributionandclassificationfollow , and Whitlock etal.(2001) Cristóbal (1960 . , ited); andGenBankaccessionnumbers( 1976 , (collector, collectionnumber, andherbariumwhere voucherisdepos- ses. Taxon sampled;geographicrangeofspecies;voucherinformation the been dispersal or vicariance Has 2006. Nowak. D. M. and D. A. Yoder, 50359 Amazonia; HM488389,HM488431; et al.3314 (GH); Brazil,northern Argentina; HM488379,HM488421; HM488405, HM488447; HM488404, HM488446. HM488376, HM488418; Sandwith; relation- Phylogenetic 2001. Baum. A. D. and Bayer , C. A., B. Whitlock, Rose; Devender 95-1037 South America, Caribbean;HM488372,HM488414; M840 HM488452. HM488410, Southwestern U.S. A., northernMexico;HM488377,HM488419. Indonesia; HM488403,HM488445; (A); Indonesia;HM488402,HM488444; (MO); Madagascar;HM488397,HM488439; (A); Malesia;HM488396,HM488438; HM488395, HM488437; Madagascar; HM488401,HM488443; America; HM488400,HM488442; pensis J. Ar.; Randrianasolo 6217 HM488435; Whitlocketal.403 (NY); Madagascar;HM488392,HM488434; B.cordifolia 8968 Rica; HM488375,HM488417.

Byttneria Byttneria Ayenia Ayenia Appendix Byttneria Byttnerieae Ayenia Byttneria Theobromeae Ayenia (GH); Americas, Tropical Africa, Tahiti; HM488394,HM488436; AnnualReviewofEcologyEvolutionandSystematics predominant biogeographicforce inMadagascar?Onlytimewilltell . SystematicBotany s.l.)basedonsequencesofthechloroplast gene, ships andfloralevolutionoftheByttnerioideae(“Sterculiaceae” or Institution. Smithsonian C.: D. Washington, Duckworth. D. W. America: acomparativereview (NY);French Guiana;HM488387,HM488429; (A);Widely distributedinSouth America; HM488380,HM488422; (NY);Brazil;HM488390,HM488432; Spruce exK.Schum.; Goldberg 76-319 Phillipson 3066 (A);Brazil,Uruguay, Argentina; HM488391,HM488433. sect. sect. sect. sect. Mori etal.11233 Cid 9705 Sagot; Byttneria (ARIZ); Argentina; HM488370,HM488412; sect. sect. sect. sect. 1 1. Specimens sampledformolecularphylogeneticanaly- (GH);Perú; HM488388,HM488430. B. catalpifolia Cristóbal; . . Rayleya bahiensis Cybiostigma Leiayenia Ayenia Cybiostigma . . . . (PERTH); Australia; HM488409,HM488451. (ARIZ);Mexico;HM488373,HM488415; Theobroma cacao Urticifolia (NY);Madagascar;HM488398,HM488440; Crassipetala Vahihara (GH); Americas, Tropical Africa, Tahiti; HM488393, Guichenotia ledifolia Byttneria (NY);Guyana;HM488371,HM488413. Prevost 3392 Lopez &Vanni 110 sp.B; (NY);Madagascar;HM488399,HM488441; (ARIZ);Mexico;HM488374,HM488416. 6 420–437. 26: .

B. microphylla Cristóbal etal.2384 A. filiformis Abroma augustum B. maingayi A. microphylla .

(NY);Brazil;HM488384,HM488426; Jacq.“South America”; A. fruticosa . Jansen-Jacobs etal.2331

Tsugaru etal.B-2500 ? . . B. biloba

.

B. coriacea B. jaculifolia Ayenia . A. magna

Cristóbal; (NY);French Guiana,Surinam,Brazil; B. divaricata L.; B. voulily , d. B J Mges E S Aes , and Ayensu , S. E. Meggers, J. B. eds. , B. implacabilis B. Rulingia magniflora S.Watson; B. morii Mast.; B. pedersenii sp. A; Jacq.; Whitlock 361 var. sp.E; B. Kleinhovia hospita (GH); Brazil,Paraguay, Argentina; Rose; B. melleri J.Gay; trnL-trnF B. sp.C; Britton; A. Gray; L.; sp.D; (L.)L.f.; Pohl; grandidieri Baill.; B. urticifolia Guiletti etal.7097 Zanoni etal.26254 (GH);Paraguay;HM488381, L.Barnett &Dorr; Benth.; Boyle etal.5550 Gentry &LaFrankie66848A Sidiyasa 1046 B. catalpifolia Jenkins 97-70 B. melleri Arnoldo-Broeders 3874 Ambriansyah etal.AA873 Cristóbal; Bc. Back.; Cristóbal; Whitlock etal.398 and (A);Brazil;HM488382, Cid andLuna3508 Laman etal.TL1378 (H; rpcl America; tropical (GH); Randrianasolo 520 Hatschbach etal.60306 A. lingulata Hansen s.n (NY);NorthernSouth A. palmeri B. schunkei Jenkins 97-71 Aèe; Arènes; Sette Silva701 Whitlock 500 matK K.Schum.; 7 405–431. 37: F. Muell.; Baker; Acevedo-Rodriguez L.; Randrianasolo 572 B. (A);Indonesia; Jacq.“Africa”; (GH);Mexico; Hatschbach etal. , respectively). , Arbo etal.6159 L.; (MO);Costa A. paniculata Whitlock 501 (US);Brazil; Watson; B. fernandesii (NY);Cuba, A. praeclara . (PERTH); . Grisebach; Schatz 2985 B. oligantha Cristóbal; Troeis etal. Miller and Mori etal. B. filipes Tressens (FTG); (GH); Wilkins B. uau- (MO); (GH); (GH); (NY); ndhF (A); (A); Van .