Copyright (c) American Society for Taxonomists. All rights reserved. Delivered by Ingenta to IP: 192.168.39.211 on: Fri, 24 Sep 2021 22:42:01 include 2009 ). Unfortunately, thephylogeneticstudies didnot and Weiblen 2004 ; Zerega etal.2005a ; floral bracts,vitreous silica,andstraightfilaments( Clement andWeiblen Datwyler acterized bythereduction ofstamennumber, peltateinter- are alsoincludedwithin , andthetribe ischar- cal genera( ies differ from thefloristic treatment inthat two neotropi- fruits” ( Berg etal.2006 ). The results ofphylogeneticstud- connate perianths,manyseededinfructescences, andfree characterized by“pistillateinflorescences mostlyformedof Baill., J. R.Forst.andG.Forst., Artocarpeae includingfivepaleotropical genera( genera includedinthetribehavechangedfrequently. cal taxawithnoclearmorphologicalsynapomorphiesandthe highly heterogeneous andunnaturalassemblageofpantropi- particularly difficult (Table 1).Ithaslongbeenrecognized asa Clement andWeiblen 2009 ), tribe Artocarpeae hasremained 1993 ; Berg 2001 ; Datwyler andWeiblen 2004 scrutiny byseveralinvestigators( ; Berg etal.2006 Berg 1977a ; , circumscription oftheMoraceae hascomeunderfrequent b ; at thetriballevelandbelow. Despitethefactthattribal Rohwer and growth formsinthefamily hascomplicateditstaxonomy rescence structures, pollinationsyndromes, breeding systems, as monophyletic,butanamazingdiversityofcomplexinflo- ( Clement andWeiblen 2009 ), thefamilyisstrongly supported 2005a ) andcombinedmorphologicalmolecularevidence Based onmolecular( Datwyler andWeiblen 2004 ; Zerega etal. regions worldwide,butits diversityiscentered inthetropics. The familyisdistributedthroughout tropical andtemperate mulberry ( as breadfruit ( eral economicallyandecologicallyimportantspeciessuch 37 generaand1,050species( Berg etal.2006 ) includingsev- DOI 10.1600/036364410X539853 © Copyright2010bythe American SocietyofPlantTaxonomists Systematic Botany The mostrecent floristictreatment ofthetriberecognizes an approximately comprises () family mulberry The series tion andpollinationare brieflydiscussedandthephylogeneticreconstructions are usedtoinformarevised treatment of Artoc phyletic lineage.We present themostcompletephylogenetichypothesisfor Artocarpeae andthegenus using maximumparsimonyandlikelihoodmethodsindicatethatnoneofthepasttreatments of Artocarpeae represent a of Artocarpeae andalsoincludedspeciesfrom severalotherMoraceaetribesandcloselyrelated familiesasoutgroups. Thedata evaluated chloroplast andnuclearDNA sequencedatafor60Moraceaetaxarepresenting allgenerathathavebeenincludedinpas netic studies,andalltreatments includehighlyheterogeneous assemblagesofgenerathatseemtorepresent across sectionof Delimitation ofthetribe Artocarpeae hasbeenparticularlydifficult. Classificationsbasedonmorphologydiffer from thoseba While itsmonophylyhasbeenwellsupportedinrecent studies,relationships withinthefamilyattriballevelandbelowre Prainea Keywords— Abstract— 4

Hullettia Old DominionUniversity, DepartmentofBiologicalSciences,110 MillsGodwinBuilding/45thStreet, Norfolk, 2

Northwestern University, PlantBiologyandConservation,2205Tech Drive,Evanston,Illinois60208,U.S. A. Cauliflori papyrifera (2010), 35(4):pp.766–782 Clarisia subgenera.Thefollowingnewcombinationsare proposed: thegenus KingexHook.f.,and Artocarpus altilis Moraceae isalarge (~1,050species)primarilytropical familywithseveraleconomicallyandecologicallyimportantspecies. or israisedto Artocarpus Ruiz&Pavón and

3 Forest Research InstituteofMalaysia,52109,Kepong, SelangorDarul Ehsan,Malaysia Pyoey n Rcrusrpin f roapa (Moraceae) Artocarpeae of Recircumscription and Phylogeny Hullettia 1 Chicago BotanicGarden, 1000LakeCookRoad,Glencoe,Illinois60022,U.S. A. , , ye J C Zerega, C. J. Nyree Clarisia Artocarpus intheiranalysesandthe place- (Parkinson)Fosberg), paper KingexHook.f., , , Vent.), andfigs( Hullettia Treculia subgenus

5 Crepnig uhr ([email protected] ) author Corresponding , , DecneexTrécul) with aFocuson Cauliflori omnctn Eio: ne Bruneau Anne Editor: Communicating 1 , 2 Parartocarpus , Virginia 23529-0266,U.S. A. 5 M N Nr Supardi, Nur N. M. Artocarpus Karsten) , , Prainea . L.). , , Treculia

766 attain enormous sizesinsomespecies,upto 100cm as insome cences are condensedcapitateheads(orrarely uniflorous latex-producing trees, orrarely shrubs. Pistillateinflores- ual infloresences. Theyare eithermonoeciousordioecious ual flowers,asdoallMoraceae, andtypicallyhaveunisex- Weiblen 2004 ; Clement andWeiblen 2009 been mostrecently includedin Artocarpeae ( ) allbearunisex- Datwyler and Hullettia, Parartocarpus,Prainea, 1B). (Fig. America and Malay PeninsulatoNewGuinea. Solomon Islands. Parartocarpus species) isrestricted totheMalaypenninsulaandSumatra. few speciesandare oflittleeconomicvalue. most recently beenincludedin Artocarpeae haverelatively are asource offoodforhumans.Theothergenerathathave (three species)occursin Africa andMadagascar, anditsseeds and for food(e.g. have beenintroduced throughout thetropics andare harvested Oceania (Fig.1A). Additionally, several what othergenerashouldbeincludedinthetribe. remains unclearisthemonophyly ofthegenus,andexactly , itsinclusioninthetribeisnotquestion,butwhat Moraceae family(after largest genusinthetribe, andthethird largest genusinthe 2001). Berg K. Schum.and Eggers, and as welladditionalneotropical ( ments alsoplaced Artocarpeae orapolyphyleticMoreae). Earlierfloristictreat- ment of . Artocarpus Artocarpus Artocarpus Clarisia A. heterophyllus Prainea 3 n ioh J Motley J. Timothy and Parartocarpus (three species),bothrangefrom CentraltoSouth Clarisia isreduced to Artocarpus isdistributedfrom Southeast Asia eastinto andthesixsmallergenera( (twospecies)rangesfrom Thailandeasttothe A. altilis

Sparattoscye Prainea Clarisia ), whichdevelopinto syncarpsandmay A. St.-Hil.)andpaleotropical ( Lam.,jackfruit). , breadfruit; wasinconsistent(eitherbeingplacedin (~45species; Berg etal.2006 ) isthe Artocarpus Ficus Artocarpus (twotofourspecies)rangesfrom the n and Bureau) genera( Rohwer 1993 ; and Batocarpus todate.Inflorescence evolu- A. camansi and subgenus 4

Batocarpus Treculia Treculia ihn Artocarpeae within Batocarpus, Clarisia, main unresolved. Artocarpus Prainea Blanco,breadnut; sed onphyloge- Ab. Aubl., L.). As thetype Decne.exTrécul were analyzed arpeae andthe the family. We tre species) (three t treatments Hullettia ) thathave , andthe mono- species × 50cm (two

Copyright (c) American Society for Plant Taxonomists. All rights reserved. Delivered by Ingenta to IP: 192.168.39.211 on: Fri, 24 Sep 2021 22:42:01 Clarisia, Treculia receptacle, andeitherhave ( remain free sothatonlyfertilizedovulesenlarge. In 2), ( Fig. flowers developseeds( Jarrett 1976 ). However, in ment oftheentire female headevenifonlyaportionofthe into ahighlyspecializedsyncarpformedbytheenlarge- face) (Fig.3).Thisallowstheentire inflorescence todevelop the apices(leavingsyncarpswithaspikyortuberculate sur- with anevensurface)orare fusedmediallyandare free at together atleastapicallyandmedially(leavingsyncarps of ( Jarrett 1959a ; Berg 1977b ) (Fig.2).Inpistillate inflorescences Clarisia which eithersitupon( cally comprisedofnumerous small,tightlypackedflowers, bose. Bothpistillateandstaminateinflorescences are typi- inflorescences are typicallyspicateorlessfrequently glo- subgenus) andB. two neotropical genera( tivated throughout thetropics. Scale barforeachmapis500km. 767 in Treculia ZEREGAET AL.:ARTOCARPUS Antiaropsis 2010] the authorsmaintainmostrecent transferofthegenustoatribeotherthan Artocarpeae ( Clement andWeiblen 2009 ). is includedin Artocarpeae inthattreatment. An asteriskmeansthegenuswasmovedtoindicatedtribe.“Maintained” (2001) included12generain Artocarpeae andtheclassificationhistoryofthese12generaislistedbelow. When Artocarpeae i Sparratosyce Sorocea Prainea Poulsenia Parartocarpus Hullettia Clarisia Batocarpus Bagassa Artocarpus Fig. Table A. heterophyllus Artocarpus Br 20 (Artocarpeae) 2001 Berg t i.*oee*ooee*oeeMaintained *Moreae *Soroceae *Moreae St.Hil. igAtcreeAtcreeAtcreeArtocarpeae(subg. Artocarpeae Artocarpeae Artocarpeae King uz&PvnAtcree*ooeeAtcreeArtocarpeae Artocarpeae *Soroceae Artocarpeae Ruiz&Pavon 1. ult*oeeGuih Srca .C eg*oeeMaintained *Moreae *Soroceae C.Berg *Moreae Gaudich. Aublet Decneex.Trecul igAtcreeAtcreeNttetdUnplaced Nottreated Artocarpeae Artocarpeae King ) orare embeddedin( Egr Csila Srca Csila Maintained *Castilleae *Soroceae *Castilleae Eggers

1. KrtnAtcree*ooeeAtcreeArtocarpeae Artocarpeae *Soroceae Artocarpeae Karsten Batocarpus, .R n .FrtrAtcreeR r roapa roapa Artocarpeae Artocarpeae Artocarpeae ArtocarpeaeR.Br. J.R.andG.Forster K.Sch.

Distribution of Artocarpeae. Thistreatment ofthetribe Artocarpeae includes: A. onepaleotropical genus( Br Csila Ataosde*atleeMaintained *Castilleae *Antiaropsidae *Castilleae Bur. BilnAtcreeAtcreeAtcreeUnplaced Artocarpeae Artocarpeae Artocarpeae Baillon Comparison oftheclassification Artocarpeae according tothefourmostrecent treatments andfindingsfrom thepresent st , theperianthsofadjacentflowersare fused ) orlack( , akri (Jret 99 95) Staminate 1975). 1959c, (Jarrett jackfruit , and Artocarpus, Prainea,Treculia, Batocarpus, Clarisia Hullettia, Parartocarpus Datwyler andWeiblen 2004 Artocarpeae *Castilleae C.Berg Hullettia, Parartocarpus Artocarpus, Prainea,Batocarpus, adjacentpistillateperianths Clarisia n and Batocarpus ) aperianth Artocarpeae *Antiaropsidae C.Berg ) afleshy . eea Several ). Treculia Prainea Berg et.al.2006

Artocarpus adjacent pistillateperianths(withthosein Artocarpus nus caul stipules,andlateralstipulescarswere placedinsubge- Those specieswithalternate,distichousleaves,nonamplexi- Malayalam word chakka given tojackfruit, stipule scarswere placed insubgenus spirally arrangedleaves,amplexicaulstipules,andannulate nized atthetimeintotwosubgenera.Specieswithalternate, vided. Trécul (1847) placedthe15speciesof twice ( Trécul 1847 ; neric taxa,but Jarrett 1959a , c , 1960a),hasbeensubdi- 1959c). ( Jarrett bracts andtheentire inflorescence enlarges intoasyncarp length. Theflowersare enclosed incavitiesbetweenthefused of theabundantinterfloralbractsare fusedforabouthalftheir adjacent pistillateperianthsare notfused,butratherthestalks Beccari (1902) notedthattheonlydifference between The smallergeneradonothave anyrecognized infrage- Pseudojaca species,including n and Clement andWeiblen 2009 Trécul. Artocarpeae *Castilleae Artocarpus Prainea A. altilis,camansi, wasthedegree offusionamong , whichhasbeenmonographed Artocarpus *Dorstenieae Gaudich. Maintained s listed,itindicatesthegenus and Jaca that inthepresent study A. heterophyllus nldn including Zerega etal. Trécul (from the Artocarpus Artocarpus A. heterophyllus of Artocarpus Prainea udy. Berg , are cul- recog- being asa ). ) Copyright (c) American Society for Plant Taxonomists. All rights reserved. Delivered by Ingenta to IP: 192.168.39.211 on: Fri, 24 Sep 2021 22:42:01 H. In in thereceptacle. F. Flowersof botanique nationaldeBelgique. of Harvard College, Archives ofthe Arnold Arboretum. FandKhavebeenmodifiedfrom Berg (1977a) withpermissionfrom the bracts. A, B–E,andGJhavebeenmodifiedfrom Jarrett 1959withpermissionfrom the Arnold Arboretum. Copyright ©Preside indicate receptacular tissue,theblackindicateseitherpistils (A –E)orstamens(GJ),andthewhite indicates eitherper are free andinterfloral bractsare present in Parartocarpusvenenosus interfloral bractsare present. DandE. genus Parartocarpus, Hullettia, [Volume 35 SYSTEMATIC BOTANY 768 Fig. A. hispidus Pseudojaca 2.

Inflorescence sections.Longitudinalsectionsthrough pistillate(A-F)andstaminate(G-K)inflorescences ofspecies (G)and ) exhibitscompletefusionofperianthapices.C. and ssp. Prainea papuana Treculia. forbesii

Treculia obovoidea and A A. Parartocarpus venenosus Artocarpus hispidus H. griffithiana (H),adjacentstaminate perianthsare free andinterfloralbractsare present. IandJ.Staminateflowersof T. acuminata are enclosedincavitiesformed bythefusionofstalksabundantinterfloralbracts.Gand lackperianthsandare embeddedinthereceptacular tissue.K. Adjacent staminateperianths . Thescalebarin A –Fis1cm,andforGK is 1mm.In A –E,andGJ,thediagonallines (subgenus ad and Prainea papuana Hullettia dumosa Artocarpus ) exhibitsmedialadjacentperianthfusion.B. exhibitsnofusionbetweenadjancentperianthapices,butdense , respectively, lackperianths,and flowersare embeddeddirectly ianth tissueorinterfloral Artocarpus dadah Artocarpus, Prainea, Bulletin duJardin nt andFellows (sub- Copyright (c) American Society for Plant Taxonomists. All rights reserved. Delivered by Ingenta to IP: 192.168.39.211 on: Fri, 24 Sep 2021 22:42:01 Subgenus eto nmlu Characteristicsshared withbothsections Section Anomalous Series of group” headingbelongtothegenus Series Series Section Series 00 ZRG TA. ROAPS 769 Subgenus His treatement wasbasedlargely onleafandstipule char- reduced thegenus Trécul’s (1847)subgenericsections( Prainea completely topartiallyfusedoneanotherandthosein ZEREGAET AL.:ARTOCARPUS 2010] Section Series Series Series Section Section Series A.heterophyllus perianth apicesfusedmediallybutfree apicallyhaveaspikysurface,like smooth surfaceasin tillate inflorescences withadjacentperianthapicesfusedapicallyhavea Table Fig. (= Jaca Laevifolii Asperifolii Incisifolii Peltati Rugosi Cauliflori Angusticarpi Clavati 3. Glandulifolium Duricarpus Pseudojaca Artocarpus Jarrett beingentirely free) ( Fig. 2 ). Renner (1907) maintained

2. ) Pseudojaca Artocarpus

Surface characteristicsof

Staminateinflorescences withvertically Interfloralbracts thinly stalkedwith Characters usedtodefineinfragenerictaxainthegenus yoemspeet lbossot Hypodermispresent; glabrous shoots Adultleavesfrequently pinnatifid;inflated (NZ6).Scalebaris1cm. Cauliflorous; absenceofresin cellsin yoemsasn;hsi hos Hypodermisabsent;hispidshoots Leafbasepinnatelynerved;noglandular Free pistillateperianthapicesfleshy; Free pistillateperianthapicesinduratedand Useilzd Unspecialized Adjacentpistillateperianthapicesfusedto

Leafbasetrinerved;glandularcrenate A. nitidus Prainea Adjacent pistillateperianthsfusedmedially, Interfloral bractsthicklystalkedwith one another;alternatedistichousleaves; Artocarpus (absent in hairs onsyncarpofsomespecies multicellular epidermal glandhairheadstypically presence ofresin cellsintheleaves; stipule scars;spongymesophyllcellsloose; amplexicaul stipulesleavingannulate apices free; spirallyalternateleaves;large peltate heads A.mariannensis globose epidermalglandhairheads of isodiametriccells,4-celleddepressed wrinkled surface,continuoushypodermis the leaves leaf margins typically unicellular compact; epidermalglandhairheads stipule scars;spongymesophyllcells nonamplexicaul stipulesleavinglateral woody; interfloralbractsabundant clavate heads crenate leafmargin long slenderstaminateinflorescences interfloral bractsinfrequent orlacking; toathird sectionwithin ssp. Artocarpus lingnanennsis A. altilis,camansi n and Characters ofgroup Artocarpus ) Duricarpus Jaca . A. Speciescontainingpis- and . (NZ4);B.specieswith

Pseudojaca , and , Artocarpus , but ), Artocarpus . A.hirsutus,nobilis,sepicanus A. anisophyllus,lanceifolius A. melinoxylus,chaplasha, A.blancoi,treculianus, A.horridus, A.scortechinii,elasticus,sericicarpus, A.heterophyllus, A.integer A.glaucus,vrieseanus,xanthocarpus, A.altissimus Sections Sections Series A. lowii,teysmannii A.petelotii,hypargyreus, A.styracifolius Series Series A. odoratissimus,hispidus,rigidus A.pinnatisectus,multifidus altilis,A.camansi, A. communis A. maingayi A. tamaran,sumatranus,kemando, A. nitidus,fulvicortex A. fretessii, A.dadah,rubrovenius, A. tomentosulus,ovatus,tonkinensis, A. reticulatus, A.lakoocha,gomezianus, A. longifolius,subrotundifolius, Incisifolii, Rugosi n Ataosde (Tbe . f h cmeig hypotheses competing the Of regarding thecircumscription of Artocarpeae, onlytwohave 1). (Table Antiaropsidae) and different tribes(Artocarpeae,Castilleae,Moreae, Soroceae, time oranotherplaceditsputativemembersinatleastfive 2004 ; Berg etal.2006 ; Clement andWeiblen 2009 authors ( ) haveatone Rohwer 1993 ; highly heterogeneous assemblageofgenera,andvarious Berg 2001 ; Datwyler andWeiblen flowers embeddedinthereceptacle. inflorescence involucre, absenceofaperianth,and pistillate Hullettia 2), andproposed forthefirsttimeacloseaffinity between vided bothsubgeneraintoseveralsectionsandseries(Table Artocarpus subgenus subgenera originallycreated by Trécul (1847) , andchanged (1907) treatment of Renner’s Artocarpus acters that Asperifolii Clavati Angusticarpi, Cauliflori, snu Jret 99 90 . l seis ptes itd ne “members under listed epithets species All 1960a). 1959c, Jarrett (sensu Objectives— Glandulifolium Artocarpus Not tested Members ofgroup and

and (recently spiltinto A. and Jaca n and rejected 1959b) (1959a, Jarrett recently, More . Peltati Prainea n and

and Parartocarpus Laevifolii Not tested tosubgenus and Historically, Artocarpeae hasrepresented a Pseudojaca Duricarpus Monophyletic Monophyleticif A. mariannensis

shared withtheothertwosubgeneraof Pseudojaca Monophyletic Monophyletic

Not monophyletic

. Jret 15c, 16a) lo subdi- also 1960a) (1959c, Jarrett ). basedontheshared presence ofan Artocarpus Nt tested Not Not tested ),

Prainea, Monophyletic Monophyletic Not monophyletic Monophyletic if Monophyletic if Monophyletic ifseries included series is exlcuded included (resulting insubgenera maintainedthetwo Cauliflori Zerega etal. A. annulatus A. sepicanus A. lowii are excluded Cauliflori is and is

Copyright (c) American Society for Plant Taxonomists. All rights reserved. Delivered by Ingenta to IP: 192.168.39.211 on: Fri, 24 Sep 2021 22:42:01 (Castilleae), L. (Cannabaceae). and Weiblen 2009 ), aswellonespecieseachof 7 SSEAI OAY [Volume 35 Ficus taxa belongtofiveothertribesofMoraceaeandonespecieseach monotypic sect. species of Clarisia, Sparattosyce,Antiaropsis Parartocarpus, 2009 ). Thus,theingroup includedtwospecieseachof Datwyler andWeiblen 2004 placed in ; Artocarpeae inthemostrecent circumscriptions ( Berg 2001 Berg etal.2006 ; ; Clement andWeiblen SYSTEMATIC BOTANY data from theplastid( or from only3–4speciesof 2004 ; Clement andWeiblen 2009 been basedonphylogeneticanalyses( Datwyler andWeiblen ). Unfortunately, samples 770 Genomic DNA wasextractedfrom approximately 1cm collected eitherinsilicagelorfrom herbariumsheets(Appendix1). (Appendix 1). previously publishedsequences;ninesequencesfor were generatedbytheauthorsforalltaxawithexceptionofseven ( Zerega etal.2002 ). sue usingamodifiedCTAB (cetyltrimethylammoniumbromide) method cycling conditionsforamplificationofthe amplification from herbariumspecimens( Taberlet etal.1991 ). Thermal and “f,”theinternalprimers“d”“e”were alsoemployedfor City, California). were run onaGene Amp PCRsystem9600(AppliedBiosystems,Foster ~50 ngofgenomicDNA). Amplification andcyclesequencingreactions 20 California), 1mg/mlBSA (bovineserum albumin),2.5mMeachdNTP, evolution andpollinationinthetribe. the genus the mostcompletephylogeneticestimatefor Artocarpeae and on theresults andmorphologicalconsiderations.We present 2) developaphylogeneticclassificationandtreatment based Artocarpus esis withwhichto:1)testthemonophylyof Artocarpeae, was designedtocreate awell-resolved phylogenetic hypoth- and nuclear(ITS125.8SrDNA)genomes,thisstudy amplified usingforward (5 1 min30sec,andafinalextensionof74°Cfor7min.TheITSregion was 3 minfollowedby32cyclesof94°Cfor45sec,52°C3072°C for in a25 ITS region were alignedusingClustal W( Chenna etal.2003 ) followed Sequencher version 3.1.2(GeneCodesCorporation, Ann Arbor, Michigan). on an ABI Prism377DNA sequencer(AppliedBiosystems)andeditedin ing products were purifiedonasephadexcolumnanddatawere collected 1 min,32cyclesof96°Cfor10sec,50°C for5sec,60°C3min.Cyclesequenc- all samplesforthe PCR reactions, buttheinternalprimers“d”and“e”were alsoemployedfor Biosystems). Primersforcyclesequencing were thesameasthose usedinthe reactions usingBigDyesequencingreagents and protocols (Applied by themanufacturer. Purifiedproducts were cyclesequencedin10 QIAquick PCRpurificationkit(Qiagen)followingprotocols provided and afinalextensionof72°Cfor7min. 50 sec,30cyclesof97°Cfor53°C72°C1min The PCRconditionsforamplificatonoftheITSregion were: 97°Cfor (modified from Baldwin 1992 ; Nickrent etal.1994 CGATGAAGAACGTAGC-3 ; Baldwin etal.1995 ). herbarium specimens,internalprimerswere alsoemployed(5 reverse (5 μ Sequence dataforthetwogeneregions (ITSandthe Taxon Sampling— DNA Extraction,Amplification,andSequencing— DNA amplificationfortheITSand Amplification ofthe SequenceAlignment andPhylogeneticAnalysis— Amplified products were purifiedwithspincolumnsfrom the Treculia M ofeachprimer, 1Mbetaine,unitTaq polymerase(Qiagen),and (Ficeae), μ l volume(1 ′ -TATGCTTAAAYTCAGCGGGT-3 Artocarpus , andinfragenericdivisionswithin were includedinthesestudies.Usingsequence Artocarpus and Dorstenia Glandulifolium trnL-F Sorocea, L.(Moreae), and aeil ad Methods and Materials × representing allsubgenera,sections(exceptthe Taq buffer with1.5mMMgCl The ingroup includedallgenerathathavebeen region. Cyclesequencingconditionswere: 95°Cfor and todate,andalsoconsiderinflorescence onespecies eachof trnL-F trnL ′ and5 Jarrett), andseries(Appendix1).Outgroup ′ Artocarpus -AACAAGGTTTCCGTAGGTGA-3 , , intron and region utilizedexternalprimers“c” Poulsenia, ′ -GCTACGTTCTTCATCGATGC-3 Sw., (Dorstenieae), trnL-F and34speciesfoursub- andnonefrom trnL-F (Maclureae (sensu Clement Hullettia, Bagassa,Batocarpus, ′ ) primers,andforsome regions were performed trnL-F Humulus region were: 94°Cfor 2 eune fo the from Sequences (Qiagen,Valencia, trnL-F ef ape were samples Leaf spacer, Artocarpus 2 ofdriedleaftis- Prainea, Treculia, L.and trnL-F are missing Hullettia Cannabis trnL-F region) ′ -GCAT ′ ) and Cerv. and μ ′ ) ) l

support ineither reconstruction. IntheMP analysis, ML and MP analysesofITS,andthese relationships haveno deep andthree tiplevelrelationships thatdiffer betweenthe past circumscriptions tobepolyphyletic.There are onlytwo the ML tree (Fig.4)revealed Artocarpeae asdefinedbyany and T=0.20520.TheMP strictconsensustree (notshown)and and basefrequencies of A =0.22130,C0.30450,G0.26900, CG =0.376200,andCT2.729000, gamma=1.2999,I0.1674, a ratematrixof AC =0.766900, AG =1.388800, AT =1.022600, from heuristicsearches hadascore of–lnL =10917.89138with evolution forITS.ThesinglemostlikelyITStree resulting able sites(GTR+IG)asthebestfittingmodelofsequence model withagammadistributionandproportion ofinvari- ( Posada andCrandall1998 ) identifiedageneraltimereversible yses atotalnumberof779characterswere used.Modeltest In thestrictconsensustree tennodescollapsed.ForML anal- consistency index(CI)of0.43,andretention index(RI)of0.66. recovered 111 mostparsimonious trees (MPTs) of1,984steps, The datamatrixhad2.6%missingdata.Parsimonysearches aligned nucleotidesofwhich416were parsimonyinformative. swapping asimplementedinPAUP* 4.01b10( Swofford 2002 ). sequence replicates, andtree bisectionandreconnection (TBR)branch a bootstrapanalysisusing1,000replicates with100randomaddition tion ( Posada andBuckley2004 ). Modeltest underthe Akaike InformationCriterion(AIC)formodelselec- joining tree asastartingtopologyandmodelparametersobtainedwith datasets. Heuristicsearches were performedunder ML withaneighbor used toselectsubstitutionmodelsthatbestfittheseparateandcombined trees. from theindependentsearches are usedtoextractthemostparsimonious weights are notassignedtothesamecharactersineachiteration.Trees characters (determinedbytheuser, 30%inthiscase)are weighted,but are equallyweighted,andonesearch inwhicha random percentage of replicate. Eachratchetperformstwosearches, onein whichallcharacters performed anditerated1,000timesperreplicate, with10trees heldper ing fewertrees perisland( Nixon 1999 ). Fivesequentialratchetruns were holding fewertrees perreplicate, samplingmanytree islands,andhold- more efficiently estimatephylogenybyrandomly varyingtaxonorder, formed withuninformativecharactersexcluded.Theratchetisableto 2002). ( Swofford maximum likelihood(ML)searches were performedinPAUP* 4.01b10 in Winclada 1.00.08( Nixon 1999 –2002) andNONA ( simony (MP)searchesGoloboff were 1999 performedusingtheratchetasemployed ) and data partitions( Hipp etal.2004 ). Separateandcombinedmaximumpar- test hasbeenshowntobeapoorofthecompatabilityseparate as there were nohard incongruences betweenthedatasets,andILD noise. We didnotemploytheincongruence lengthdifference test(ILD), reconstruction, allowingthephylogeneticsignaltoassertitselfover a scenariomayleadtobetterresolution andmore accuratephylogeny branching histories( Seelanan etal.1997 ). Combiningthedatainsuch character evolutionandresolution intheother, ratherthandifferent or bothofthedatasetsleadingtoanunstablepositionandconsiderable soft incongruences, conflictslikelyreflect insufficient informationinone strap supportfornodesinbothoftheseparateanalyses.Incase or higher)soft(bootstrapbelow70%)incongruences basedonboot- trees obtainedforeachregion were examinedforhard (bootstrapof70% their nucleotidesequencedidnotvary. repeat. Indelswere treated asthesamestateiftheywere thesamesizeand of unambiguouslyalignednucleotidesandwere notasinglenucleotide as additional,unordered charactersiftheywere bordered bystretches in Se-Alv2.0a7b( Rambaut 2001 ). Forthe aligned manually. Manualalignmentandoptimizationwere performed by manualoptimization.Sequencesfrom the T Analyses— ITS Clade supportforbothMP andML phylogenieswere assessedwith For ML analyses,Modeltestversion3.7( Posada andCrandall 1998 ) was Maximum parsimonysearches usingtheratchetmethodwere per- Data from ITSandthe The ITSdatasetprovided atotal of779 trnL-F Results regions were analyzedseparately. The trnL-F region, indelswere coded trnL-F region were easily Maclura Copyright (c) American Society for Plant Taxonomists. All rights reserved. Delivered by Ingenta to IP: 192.168.39.211 on: Fri, 24 Sep 2021 22:42:01 are indicated bysymbolsonbranches:Gray circles =90–100%,black circles =80–89%,graysquares =70–79%,andblack squares 771 ZEREGAET AL.:ARTOCARPUS 2010] Fig. 4.

Maximum likelihoodanalyses basedonseparatedatasets. A. Tree basedonITSdata, B.Tree based on trnL-F data.Bootstrapsupportranges 60–69%. = Copyright (c) American Society for Plant Taxonomists. All rights reserved. Delivered by Ingenta to IP: 192.168.39.211 on: Fri, 24 Sep 2021 22:42:01 bootstrap) assisterto uana ( Fig. 4 ). There was98%supportforplacementof provided weakornosupport foranalternatearrangement support foranarrangementoftaxawhiletheotherdataset tion offourinstanceswhere onedatasetprovided strong minor rearrangements at unsupportedtips,withtheexcep- on theseparateanalysesofITSand 4). (Fig. group ML analysis,thesetaxaformanunsupportedmonophyletic was strongly supported(96%)aspartofacladeincluding Dorstenieae asdefinedhere) intheITStree. lactescens, Treculia obovoidea, (all membersofCastilleae)and ses, respectively. For ML analysesofthecombined dataset compared with 25and16nodesintheITS and the combinedanalysis,35nodes hadsupportof70%orhigher, combined analysiscompared toeitherseparateanalysis. In Additionally, thenumberofsupportednodesincreased inthe consensus tree, sevennodescollapsed(MP tree notshown). MPTs of1,992steps,CI=0.43,andRI =0.65.Inthestrict Parsimony searches ofthecombineddatasetsrecovered 16 relationships were present, thetwodatasetswere combined. sister relationship intheITStree. As nohard incongruencies in the Batocarpus sister tothebreadfruit clade(withnosupport)intheITStree. members ofseries in the position wasunresolved within the [Volume2) 35 the a K81uf+Gasthebestfittingmodelofsequenceevolutionfor were used.Modeltest( Posada andCrandall,1998 ) identified lapsed. ForML analyses,atotalnumberof1,140characters 0.89. Inthestrictconsensustree (notshown)26nodescol- searches recovered 552MPTs of202steps,CI=0.75,andRI SYSTEMATICindels whichwere codedasseparatecharacters.Parsimony BOTANY region provided fiveunambiguousparsimonyinformative data matrixhad13.7%missingdata. Additionally, the nucleotides ofwhich123were parsimonyinformative.The A.petelotii. 1) ML analysis,thefollowingtaxaformagradeofthree clades: Prainea, Batocarpus,Clarisia,Morus,Sorocea, ML analysis,itissistertoacladecomprisingonly pomifera 772 Antiaropsis decipiens,Sparattosycedioica, F a gradeofthree clades:1) MP analysis.IntheMP consensustree thefollowingtaxaform 0.31930. TheML frequencies of A =0.35970,C0.16200,G0.15900,andT CG =0.825400,andCT1.832000,gamma1.2094,base a ratematrixof AC =1.010600, AG =1.832000, AT =0.396900, from heuristicsearches hadascore of–lnL =3,905.04799with and involveminorrearrangements of between theML andMP analysesofITSare nearthetips unsupported monophyleticgroup. Theremaining differences In theMP analysis,thesecladesare partofanunresolved and Antiaropsis, tree, anditwassistertoacladecomprising Cmie Analyses— Combined tn- Analyses— trnL-F Dorstenia, Brosimum, Ficus trnL-F trnL-F inacladewith trnL-F and issistertotherest oftheMoraceaefamily, whileinthe dataset.Thetwomostlikely tree, but there wasnobootstrapsupport fortheir n and

and Castilla tree. Clarisia Sparattosyce trnL-F Rugosi Ficus carica ; and3) h The Prainea limpato and were supported(88%)assistertaxain Castilla elastica topologywasmore resolved thanthe trnL-F inthe Comparing thephylogeniesbased Treculia Dorstenia, Brosimum, , and3) Hullettia and wasstrongly supported(95% datasetprovided 1,140aligned Dorstenia choconiana,Brosimum trnL-F T. africana , 2) Hullettia Artocarpus intheITStree, whileits and (Castilleae)inthe Ficus, Castilla,Poulsenia, tree andwasplacedas Artocarpus camansi and trnL-F trnL-F Parartocarpus and and (allmembersof Poulsenia armata Artocarpus lowii revealed only + trees resulting Castilla elastica, Bagassa Parartocarpus and trnL-F Prainea Prainea pap- Artocarpus, Treculia . Inthe analy- . Inthe trnL-F clade trnL- and , a ; .

and inwhether bootstrap) or exact placementof and MP trees basedoncombineddatasetsdiffered onlyinthe 0.586, andproportion ofinvariablesites=0.2477.TheML 0.29870, C=0.23990,G0.21290,andT0.24850,gamma CG =0.558200,andCT2.416800,basefrequencies of A = rate matrixof AC =0.674700, AG =1.243500, AT =0.557300, heuristic searches hadascore of–lnL =15,459.66603witha and fitting modelofsequenceevolutionforthecombinedITS and aproportion ofinvariablesites(GTR+IG)asthebest a generaltime-reversible modelwithagammadistribution were used.Modeltest( Posada andCrandall1998 ) identified which todiscusstheresults. tribal leveltreatment willbeusedastheframeworkwithin Clement and Weiblen (2009) , withonlyafewdifferences, their largely agree withthemostrecent Moraceaetreatment of several tribesoftheMoraceae( Table 1 ). Becauseourresults the taxaonceplacedwithintribeare spread throughout classifications represent amonophyleticgroup, butrather sented here indicatethatnoneoftheprevious Artocarpeae referred tointhefollowingdiscussion( Fig. 5 ). Thedatapre- tionships, theML tree basedonthecombineddatasetswillbe and ML analysesvariedonlyintwopoorlysupportedtiprela- and thephylogeniesbasedoncombineddatasetsforMP molecular datasetspresented here hadnosignificantconflict, Berg etal.2006 ; Clement andWeiblen 2009 ). Becausethetwo recent treatments ( Berg 2001 ; by includingallgenerathathavebeenplacedinthetribe Datwyler andWeiblen 2004 ; been variable.Thisstudytestedthemonophylyoftribe has historicallybeendifficult andcircumscriptions have timing andmechanismsforthemovementofthisgroup. aid intestingthishypothesisandfurtherunderstandingthe Artocarpeae phylogeneticreconstruction presented here will Landbridge ( Zerega etal.2005a ). Themore comprehensive the OldtoNewWorld across anEoceneNorth Atlantic and thattheirsplitwasfacilitatedvialandmigrationfrom lineages diverged from oneanother65.1mya(52.2–80.6mya) divergence dateestimates forMoraceaesuggestthatthese Malesian lineage( lineage ( here comprisesthree genera,whichincludeasmallneotropical Artocarpeae and deposited inTreeBASE (studynumberS2347). bootstrap) (Fig.5).Datamatricesandtrees forthisstudyare total of1919characters(779from ITSand1,140from 20) (Tbe 1). (Table (2009) by Datwyler andWeiblen (2004) and As such,wemaintainthetreatment ofCastilleaeasproposedClement andWeiblen encloses theflowers(asopposed tofullyenclosinginFiceae). inflorescence involucre ofimbricatebractsthatonlypartially synapomorhpies thatcharacterizeCastilleae,namely an as partoftheCastilleaeclade andallthree generashare the present studyresolved the Moraceaefamily( Rohwer 1993 ; Berg 2001 ) ( been placedinthetribe Artocarpeae inrecent treatments of Table 1 ). The Castilleae— Phylogeny— Artocarpeae This studyrepresents themostcomplete phylogenyof trnL-F Batocarpus dataset.Thesinglemost likelytree resulting from Bagassa Antiaropsis, Morus Artocarpus n and A. fulvicortex Artocarpus issisterto issisterto Antiaropsis, Sparratosyce, Clarisia Discussion

Sparattosyce, todate. Artocarpeae astreated h dlmtto o Artocarpeae of delimitation The nldn including ) andalarger Southeast Asian/ withinsubgenus Morus Bagassa and + + Sorocea Prainea Sorocea Poulsenia and (ML,100% ) Previous ). Pseudojaca (MP, 61% Poulsenia trnL-F have )

Copyright (c) American Society for Plant Taxonomists. All rights reserved. Delivered by Ingenta to IP: 192.168.39.211 on: Fri, 24 Sep 2021 22:42:01 circles = 60–69%. scored for thesecharacters.Bootstrapsupport rangesare indicated bysymbolsonbranches:Blackcircles =90–100%,graycircl nate flowers.The tree ontherighttraces the degree offusionamong perianthsfrom adjacent flowersinpistillateinflorescen 773 ZEREGAET AL.:ARTOCARPUS 2010] Fig. 5.

Maximum likelihoodtree basedoncombineddatasetsfrom ITSand trnL-F . Thetree onthelefttracesnumberofstamens instami- ces. All specieswere es =80–89%,open Copyright (c) American Society for Plant Taxonomists. All rights reserved. Delivered by Ingenta to IP: 192.168.39.211 on: Fri, 24 Sep 2021 22:42:01 7 SSEAI OAY [Volume 35 SYSTEMATIC BOTANY 774 apart from Ficeae. cences, whichare typically notfoundinotherMoraceaetribes However, mostgenerainthetribehavebisexualinflores- of habitsfrom herbs,tosucculent shrubs, totrees ( Berg 2001 ). quite variable,beingtheonlytribethatexhibitsfullrange the placementof the fusedinterfloralbractstalksof or thefusedadjacentpistillateperianthsof ded inrecaptacular tissue (e.g. tion ofcharacterhomologies(i.e.confusingflowersembed- placement issurprising.Itpossiblethatamisinterpreta- with Dorstenieaehaveneverbefore beenconsidered, andthis in inflorescences, infructescences, fruits, andseeds, affinities ance between (1962) and Berg (1977b) numerous African andMadagascanmembers.While bothhypothesizedapossiblealli- Corner strong supportwithinthetribeDorstenieae,awith in previous circumscriptions of Artocarpeae, isnestedwith study indicatesthat Weiblen 2009 ) didnotincludeany ( Datwyler andWeiblen 2004 ; Zerega etal.2005a ; Previous phylogeneticstudiesbasedonmoleculardata Clement and tribe thatcombinedthe Artocarpeae andMoreae tribes. and Datwyler African Moraceae, 2001; Berg (1977b) Berg placed 1993; Weiblen Rohwer 2004 ; 1962; Berg etal.2006 Corner ). However, inhistreatment of 1959a ; has beenprimarilytreated in Artocarpeae eversince( Jarrett Trécul’s (1847)monographictreatment of Artocarpeae, andit the present studysupportsthis. ( Datwyler andWeiblen 2004 ; Clement andWeiblen 2009 ) and recent treatments ofMoraceaeplacethesegenera in Moreae the tribe Artocarpeae ( Rohwer 1993 ; Berg 2001 ). Themost first proposed acloserelationship between about itsrelationship totheothergenera. Jarrett (1959a) the Artocarpeae and Conocephaleae, andwasuncertain Renner (1907) excludedthegenusfrom histreatment of erroneous placementofthegenusinConocephaleae. position of 2004 , Zerega etal.2005a ; not beenincludedinthesestudies( Clement and WeiblenDatwyler andWeiblen 2009 ). The either Moreae or Artocarpeae, while recorded conflictingplacementsof Berg 2001 in ; Artocarpeae inrecent floristictreatments ( Jarrett 1960b Berg etal.2006 ; ). Phylogeneticstudies have to Dorstenieae. with Dorstenieae.We recommend that ducted tohelpelucidatethisintriguingaffinity of morphological, anddevelopmentalstudiesshouldbecon- rescences withinthetribe Dorstenieae.Furtherphylogenetic, lineage mayrepresent anincompletelossofbisexualinflo- rescences frequently occur( Jarrett 1959a ; have pistillodes,andinonespecies, Berg 1977b ). This numerous abortivemale flowers, maleinflorescences often cies. However, thefemaleinflorescences of includes bothdioeciousandmonoeciousshrub andtree spe- that isabsentin sue. Thetwo genera alsoshare aninflorescence involucre of perianthsandflowersembedded inreceptacular tis- strap) bythisstudy)based in partontheshared absence Parartocarpus Moreae— Dorstenieae— Unplaced— Hullettia Bagassa (arelationship strongly supported(100%boot- Parartocarpus Treculia Treculia Artocarpus Treulia Treculia and hasbeeninquestionsinceKing’s(1888) Treculia and wasestablishedbyDecaisne in in Artocarpeae. TheDorstenieaeare Sorocea isa small genus(three species)and Parartocarpus and . Theresults presented here sug- , theonly African taxonincluded havebothbeenplacedin Hullettia Hullettia Treculia Treculia T. africana, Hullettia Treculia Parartocarpus basedonsimilarities Treculia and species.Thepresent havebeenplaced ) mayhaveledto Treculia Artocarpus bisexualinflo- Parartocaarpus betransferred sampleshave Hullettia inaMoreae mayhave within Treculia with and )

The thick-walled medialportionsoftheperianths become adjacent pistillate perianthsare entirely free from oneanother. pistillate inflorescences of pistillate perianths.Interestingly, Jarrett notedthatinyoung gested that tions existinallofthetribes. ber ofstamensperflowerintheMoraceaeisfour, butexcep- more typicaltwotofiveinotherMoraceae.Thenum- one tothree in Clarisia as separategenera.Furtherstudiesfocusingonallspeciesof become betterknown,theymayprove difficult tomaintain one anotherandthatasthespeciesofthesetwogenera bootstrap) cladeof strap) cladethatissistertothemore weaklysupported(65% (1907) viewed a closeone( Beccari 1902 ; Renner 1907 ; between Jarrett 1959a ). Renner limits. one (orlessfrequently twoin 5). ( Fig. ported byareduction instamennumberwithinthefamily in thesefourgenera. Artocarpeae asdefinedhere are sup- Artocarpeae bereduced tocomprisethespeciesrepresented in thecurrent studyanditisrecommended thatthe limitsof 2009 ). Thisplacementisstrongly supported(100%bootstrap) 2001 ; Datwyler andWeiblentreatments ofthefamily( 2004 Jarrett 1959a ; ; Clement andWeiblenhave allbeenplacedin Artocarpeae inoneormore recent Rohwer 1993 ; Berg further studiesare warranted. to three closelyrelated tribesinthisandprevious analyses, tus. However, giventheclade’sunstablepositioninrelation clade of relationship. Basedonourresults, thestrongly supported + CastilleaeDorstenieae,butthere isnosupportforthis gest that exception of and resin-containing cellsintheleafmesophyll(with both haveglandularepidermalhairswithmulticellularheads with subgenus genus of fusionamongadjacentpistillateperianthsin genus. Jarrett (1959a) treated placedpriorityon reproductive (lack 1959b) (1959a , the subgenericlevelwithingenus subgenera lotaxy andstipulecharacters(which vegetative characters.Rennerplacedpriorityonleafphyl- pared topartialcomplete fusioningenus within thegenus cies sampled)issupportedasamonophyleticgroup nested treatment, as supports Renner’s phyll. Thecombinedphylogeneticevidencepresented here gland hairheadsandnoresin-containing cellsinthemeso- ter), whereas subgenus was basedprimarilyonthedegree offusionamong adjacent subgenus of between othersubgeneraof the combinedphylogenyanditsmorphologicalintermediacy Batocarpus Atcru ad rie Phylogeny— Prainea and Artocarpus Artocarpeae— The treatment of Pseudojaca n and Artocarpus, Prainea,Clarisia, Hullettia Artocarpus Hullettia Jaca Clarisia Batocarpus n and Artocarpus A. heterophyllus Prainea (= Clarisia Artocarpus Batocarpus ), andleafanatomy(which and Clarisia Artocarpus and Artocarpus Prainea n and n and Artocarpus asanintermediate between ) stamenperflowerascompared tothe willbenecessarytodetermine generic Prainea . Parartocarpus Parartocarpus Pseudojaca Batocarpus Prainea formawell-supported(100%boot- . ). asaseparate genus(Jarret 1959a,b) , A. rigidus and Prainea . Giventheposition of ad and ) Clarisia, Prainea Artocarpus, Batocarpus asaseparatebutcloselyallied + haslongbeenrecognized as A. integer Prainea. hasunicellularepidermal Pseudojaca Prainea havecloseaffinities with and subgenus maydeservetribalsta- and maybesistertoFiceae Prainea (subgenus Artocarpus, n and it istreated here asa obr (92 sug- (1942) Fosberg (twooffourspe- Batocarpus whichlackthelat- h relationship The shares withsub- A. annulatus , and andplaceditat Artocarpus Prainea while Jarrett Prainea Artocarpus Artocarpus Artocarpus Artocarpus Prainea l have all shares over ) com- , and , in , )

Copyright (c) American Society for Plant Taxonomists. All rights reserved. Delivered by Ingenta to IP: 192.168.39.211 on: Fri, 24 Sep 2021 22:42:01 al 2; Fg. ) Sre Series 3). 2, Figs. 2; ( Table Artocarpus etic group (100%bootstrap).Itiswelldefinedwithinthegenus ( Table 2 ). Section Glandulifolium two sectionswithinsubgenus series levelthere isvaryingsupportasdiscussedbelow. logeny presented here. Additionally, atthesectionaland et al.(2006) , are notentirely supportedbythecombinedphy- tained by Renner (1907) Pseudojaca Jarrett (1959a , c , 1960a), and Berg 775 and wouldbeofinterest forfurtherinvestigation. nomenon amongangiosperms( Okimoto 1948 ZEREGAET AL.:ARTOCARPUS , Moncur 1985 ) Delayed fusionofneighboringpartsisarelatively rare phe- has secondarilylosttheabilitytoundergo delayedfusion. sible that and subsequentenlargement oftheground tissue. Itispos- the perianthbeginstothickenoutward duetorapiddivisions ied. Hefoundthatevenbefore anthesisthemiddleregion of free from oneanotheratearlystagesinalleightspecies stud- Pseudojaca cies (sevenfrom subgenus ied theanatomyandmorphologyofeight in fusion ofthemedialportionadjacentpistillateperianths fused onlylaterindevelopment. Moncur (1985) alsoreported 2010] was sistertosubgenus (as theposition of ses of11 speciesfoundneithersubgenustobemonophyletic based onrestriction fragmentlengthpolymorphism analy- in thisanalysis. A previous tested sinceonlyone( no support,whilethemonphyly ofseries series ( Table 2 ). Thetwosubgenera, shares themostmorphological characters. it istreated here withinsubgenus lack ofsupportforitssisterrelationship tosubgenus et al.2004b , 2005b ). Givenitsproblematic positionandthe fruit cladeare knowntohybridize ( Fosberg 1960 ; tion israrely reported in Zerega in subgenera possible but isconsistentwithsubgenus style andtheventralhilum,whichisunusualin Artocarpus sepicanus In thephylogenybasedon a cladecontainingsubgenus 1959b ). InthephylogenybasedonITS, of well-developedinterfloralpeltatebracts)( Table 2 (long slendermaleinflorescences) and ) ( Jarrett because itshares characterswithbothsections has beentreated asanomalouswithinsubgenus nus of resin inthespongymesophyll cellsclearlymatchsubge- adjacent pistillateperianths(withapicesfree), andpresence atic. Itsleafarrangement,stipulecharacters,partialfusionof any supportandthepositionof is sistertosubgenus the genus within acladecomprisedofsubgenus Atcru Sbeu Pseudojaca— Subgenus Artocarpus Sister tosubgenus Artocarpus A. heterophyllus Artocarpus A. sepicanus Prainea Artocarpus. , originallydescribedby Trécul (1847) andmain- ), andreported thatadjacentpistillateperianthsare bybothvegetativeandfloralsynapomorphies hasbeendividedintosubgenera,sections,and (notincludedinthisanalysis)and Prainea , ratherthansubgenera represents alineagewithin Pseudojaca onlyafteranthesis. Sharma (1965) stud- A. nitidus hasawideseparationofthesubapical isofhybridoriginwithputativeparents Inthecombinedphylogeny, Prainea Prainea A. petelotii and Pseudojaca Peltati Artocarpus Artocarpus hasstrong support asamonphyl- Artocarpus wasunresolved and isthespecies . Noneoftheseplacementshave Prainea Artocarpus trnL-F ) ofthree specieswasincluded ismonophyletic,thoughwith A. sepicanus ) ( Kanzaki etal.1997 ). Prainea Pseudojaca plussubgenus Artocarpus , membersofthebread- , , andonefrom subgenus art (90) described (1960a) Jarrett Artocarpus Atog hybridiza- Although . A. sepicanus hlgntc analysis phylogenetic Prainea A. sepicanus Pseudojaca Duricarpus ( Jarrett 1959a ). Itis Clavati A. sepicanus, remains problem- te monotypic the : Artocarpus , withwhichit andtherest of Artocarpus = (= couldnotbe A. chaplasha A. sepicanus r or Artocarpus, Pseudojaca. issisterto Artocarpus Artocarpus (presence collapses Pseudojaca Jaca Prainea Prainea. which ) and ) spe- that ,

breadfruit cladeserving asthematernalparent and amember that ter tobreadfruit anditsrelatives basedonITS.Itispossible varies, beingnestedwithin in Table 2 . Thepositionof all thespeciesinthiscladehave thesynapomorphieslisted phyletic if as anomalous.Series tion cies discussedabove. raised tothesubgenericrankandcomprisesthree spe- rous ( Kochummen 2000 ). Inthetreatment below, The inflorescences of than theinduratedperianthapicesofsection ous perianthapices,indicativeofsection latus from afewlocalities. Berg etal.(2006) considered Artocarpusannulatus with thesespeciesasisterrelationship to but present studyindicatesthat lus ined in cells (absentin mesophyll andtheabsenceofresin inthespongymesophyll this sisterrelationship. Members of They are alliedwithsubgenus medially fusedbutfree apically) withsubgenus perianth fusioncharacters(adjacentpistillateperianths ment (spirallyarrangedwithamplexicaulstipules)and rescences mayalsobeaxillary. Theyshare theleafarrange- synapomorphy ofcauliflorous inflorescences, thoughinflo- etic (100%bootstrap)and,asthenamesuggests,share the series withintwosections( those insubgenus Artocarpus ral synapomorphies( Table 2 ; Figs. 2 has beendefinedwithinthegenusbybothvegetativeandflo- , 3 ). Speciesinsubgenus present study. are addressed inthetaxonomictreatment belowinlightofthe treated differently by Berg etal.(2006) , andthesedifferences included. Among these,severalhavebeensubsequently In thepresent study, ninespeciesandfoursubspecieswere ous subspecies)withinsubgenus etic group, ifseries represents astrongly supported(100%bootstrap)monophyl- The datapresented here indicatethatsubgenus nus monophyletic ( Figs. 4 , 5 and ). Series Section are flexuousratherthan indurate asinsection strap supportand ( Jarrett 1959c ) are monophyletic( ces ( Figs. 3 , 5 ). Theseriesdescribedwithinsection ical synapomorphyofindurate,free, pistillateperianthapi- bootstrap), andmembersofthesectionshare themorpholog- are excludedfrom it. The remaining speciesthat Jarrett (1959c) includedinsec- Jarrett (1960a) recognized 19species(severalwithnumer- Atcru Sbeu Artocarpus— Subgenus Artocarpus Scin Section In section (jackfruit) and A. annulatus Pseudojaca A. sepicanus tobepartofsection A. lowii Artocarpus A. annulatus Artocarpus Duricarpus exhibitmuchgreater morphological diversitythan A. lowii maybeofhybridorigin, withamemberofthe Artocarpus + were inseries hadnotyetbeendescribedatthetime.The ) isstrongly supported(100%bootstrap)as A. heterophyllus Prainea. Pseudojaca isincludedwithin it. Apart from Laevifolii A. integer (withtheremoval ofseries Cauliflori ismonophyleticwithweaksupport(60% isendemictoSarawakandknown only ). Jarrett (1959c) included A. annulatus Rugosi , thefree, pistillateperianthapices However, there isnosupportfor Duricarpus Duricarpus with61%bootstrapsupport). (chempedak)inseries A. lowii A. annulatus , and Jarrett (1959c) describedsix andtheanomalous isweaklysupported asmono- Rugosi Pseudojaca Rugosi and Cauliflori canbeaxillaryorcauliflo- Asperifolii basedon intheseparateanalyses Pseudojaca and Cauliflori . However, it has flexu- , , A. integer, Incisifolii ugns Subgenus isalsocloselyallied Artocarpus inhavingcompact issistertosubge- Artocarpus with82%boot- are monophyl- trnL-F eis series A. heterophyl- orclassified nt exam- not A. sepicanus Duricarpus Duricarpus Cauliflori Artocarpus. Duricarpus A. integer Artocarpus Artocarpus ) ( Table 2 ). 2). (Table ) Cauliflori, Cauliflori andsis- A. annu- A. lowii rather , Peltati is . , . . .

Copyright (c) American Society for Plant Taxonomists. All rights reserved. Delivered by Ingenta to IP: 192.168.39.211 on: Fri, 24 Sep 2021 22:42:01 7 SSEAI OAY [Volume 35 SYSTEMATIC BOTANY of the 776 within section The combinedphylogenystrongly supportsitsplacement indurate, free, perianthapices typicalofsection der, maleinflorescences typicalofsection discussed above.Inthecaseof Artocarpus characters thatappeartobeintermediatebetweensections (1959c) didnotassigntoasection,aseachspeciespossesses mine theaffinities of additional dataandsamplesshouldbeexaminedtodeter- Primack 1983 ; Momose et al. 1998 ; Sakai etal.2000 cies, are). However, mixed ( Corner 1962 ; Singh etal.1963 ; Artocarpus Brantjes 1981 ; Artocarpeae, onlylimiteddata existonpollinationforafew 2004a ), theinflorescence structures mayprovide clues.Within Momose etal.1998 ; Sakai etal.2000 ; Artocarpus, Sakai 2001 ; Zerega etal. 2005 ). the efforts toward aphylogeneticclassification( Rønsted etal. vergent evolutionwithinthegenusthatcontinuetoconfound of wasppollination,andthere are numerous examplesofcon- inflorescence showsclearadaptationstothespecializedmode in reproductive strategies.In throughout thefamily, butmaybeindicativeofthediversity rescences andinfructescences hasconfoundedclassification of function,andparallelevolution.”Thisdiversityinflo- many fascinatingproblems ofvestigalfeatures, transference sishing arrayofinfructescences” andthatMoraceae“holds ily hassuchsmallstandardized flowers,yetsuchanaston- writing aboutMoraceae, Corner (1962) statedthat“Nofam- this species. before more definitiveconclusionscanbereached about Examination ofadditionalplantmaterialwillbenecessary ing dataorhybridoriginwithparents from eachsection. Artocarpus subgenus lis was successfullysequencedforthisspecies.When in thephylogenieshere asonlythe tion but well-developedpeltateinterfloralbractstypicalofsec- slender maleinflorescences typicalofsection species ( described inthetaxonomictreatment below. scriptions inthisseriesandtheyare notmaintainedhere, as Berg etal.(2006) madeseveralchangestospeciescircum- indicates itdoesnotrepresent anaturallineage. Additionally bers originallyincludedinseries Moraceae family. Thepresent studydoesnotincludeallmem- labile nature ofleafshapeinthisgroup andthroughout the anisophyllus era exhibitpinnatelylobedjuvenileleaves.Onespecies( leaves withentire margins, severalspeciesinboth subgen- While consistent presence ofpinnatifidadultleaves( Jarrett 1959c ). heads asintherest ofthegenus)andonoccasionalto epidermis (asopposedtoeithergloboseordepressed globose multicellular peltateheadsontheglandularhairsofleaf wasincludedintheanalyses,italways occurred within Sre Series Although pollination inothergeneraofMoraceae,like Inflorescence EvolutionandPollinationBiology— Within subgenus Duricarpus Rugosi Artocarpus Incisifolii A. hirsutus,sepicanus species,andtheconclusions,evenwithinaspe- Artocarpus n and n and hasreceived lessattention(vanderPijl1953; ) evenhascompoundleaves,demonstratingthe cladeservingasthepaternalparent. However, Duricarpus Duricarpus Duricarpus. . Theplacementof speciesoutsideofthisseriesallhaveadult wascircumscribed basedonthepresence of A. lowii Artocarpus , butcausedtheresolution ofsections . . tocollapse,possiblyduemiss- Thepositionof Artocarpus nobilis . Ficus there are three anomalous A. hirsutus, , and , forexample, thesyconium Incisifolii A. nobilis A. nobilis trnL-F Artocarpus , butnonetheless ithaslong,slen- A. sepicanus alsohaslong, spacerregion isnotshown ) that Jarrett Duricarpus Artocarpus bt has but , A. nobi- When was A. . , including ( a monophyletic Artocarpeae comprisingtwoneotropical ing morphologicalcharacters,thistreatment circumscribes phylogenetic analysesofmoleculardata,andconsider- 2006 ; Clement andWeiblen 2009 1993 ). Basedonevidencefrom ; Berg 2001 tribe withinMoraceae( ; Corner 1962 ; Datwyler andWeiblen 2004 long beenaheterogeneous, ill-defined,andever-changing Jarrett 1959a ; ; Berg etal. Rohwer interpret pollinationinanevolutionarycontext. genetic classificationwillbeausefultooltounderstandand studies willbenecessaryforfurtherelucidation,andaphylo- dromes in Artocarpeae are stilllargely unknown,empirical ing easyaccesstotheovules.Itisclearthatpollinationsyn- Duricarpus and geal germination (semihypogealin Members of Artocarpeae alsoshare straightembryos,hypo- flower, withafew speciesoccasionallyhaving1–3stamens. in Artocarpeae typically haveonlyonestamenperstaminate typical numberofstamensin Moraceaeis4or5,butspecies cies havealsoindependently evolvedasinglestamen).The compared totherest of thefamily(althoughseveral synapomorphy forthetribeis areduction instamennumber be free orpartiallytocompletelyfusedoneanother. The flowers with2–4connatetepals,andadjacentperianthsmay pistillate inflorescences haveonetomore typicallynumerous (occasionally 2–3maybepresent) thatisstraightinbud.The flowers with2–4connatetepals,andtypicallyonestamen ent orabsent.Thestaminateinflorescences havenumerous cauliflorous inafewspecies.Interfloralbractsmaybepres- inflorescences are unisexual,andare typicallyaxillary, butare and haveeitheramplexicaulornonamplexicaulstipules.The are simple(rarely compound),spirallyalternateordistichous, climbers, andare eithermonoeciousordioecious.Theleaves I. Berg etal.2006 ). described indetailelsewhere ( Jarrett 1959c , 1960a ; changed, descriptionsare notincludedastheyhavebeen Berg 2001 ; of thegroup are included.Whencircumscriptions havenot era, briefdescriptionsthathighlighttheuniquecharacters circumscriptions havechanged withinthe Artocarpeae gen- status, and Hullettia recent circumscriptions of Artocarpeae: due tothefusionofadjacentperianths(subgenera Artocarpus from predators. Additionally, thepistillateinflorescences of with amplepollenforlarvaeandopportunitiesofprotection provide apotentiallyattractivebreeding sitefor insects, tightly packedflowers,andfrequently withinterfloralbracts, 2006 ). In 2000 ; Sakai 2001 ; Artocarpus Berg 2001 ; Zerega etal.2004a deceit, maybemore commonthanpreviously realized in ; Berg etal. inflorescences, andvisitingpistillateinflorescences through pollination byphytophagousinsects,breeding instaminate Clarisia Artocarpeae Txnmc ramn o Artocarpeae— of Treatment Taxonomic Members of Artocarpeae canbetrees, shrubs, orrarely (Parkinson) Fosberg. 3(8): 108.1847,nom.inval.—TYPE: 454. 1818. Pseudojaca n and formamonophyleticgroup thatmaywarranttribal Artocarpus are wellprotected againstphytophagousinsects andotherMoraceae(vanderPijl1953; Sakai etal. andsubgenera Prainea Treculia Batocarpus ), orinsomecasesinterfloralbracts(section Euartocarpeae R.Br. inTuckey, Narr. Exped.Zaire, App. 5: ) genus.Three generaare removed from istransferred toDorstenieae.Whentaxon , staminateinflorescences withnumerous ) andonepaleotropical ( Trécul, Ann. Sci.Nat.,Bot.ser. Pseudojaca Clarisia n and and notexamined Parartocarpus roapa has Artocarpeae Artocarpus altilis Prainea Artocarpus Artocarpus Ficus ) deny- ), and spe-

Copyright (c) American Society for Plant Taxonomists. All rights reserved. Delivered by Ingenta to IP: 192.168.39.211 on: Fri, 24 Sep 2021 22:42:01 another (subg. (subg. ers, adjacentperianthsmaybe free (subg. inflorescences: withnumerous tightlypackedtubularflow- (-4) connatetepals,stamens 1(-3), straightinbud.Pistillate inflorescences: withnumerous tightlypackedflowerswith2 (subg. Prainea Paleotropics ( 2001 ). and large seeds( examined in 1. Staminateinflorescences spicatetogloboseobovoidorclavate,lackingadistinctabaxialsterilestrip;staminate and and and pound – Sitodium A.Artocarpus 777 ZEREGAET AL.:ARTOCARPUS 1. Staminateinflorescences spicatewithadistinctabaxialsterilestrip;staminateflowerscrowded inlongitudinalrow in 2010] (dioecious insubgenus Prainea Polyphema Radermachia Distribution— Trees (possibleclimberinsubgenus Batocarpus 3. Perianthsofadjacentpistillateflowerspartiallytocompletelyfusedformasyncarp;entire pistillate 3. Perianthsofadjacentpistillateflowersentirely free from oneanother;onlyfertilizedflowers 2. Inflorescences oftencauliflorous, orifaxillarythenthebarkatbaseoftrunk reddish; pistillateinfloresce 2. Inflorescences axillary;pistillateinflorescences multiflorous andglobose-capitate;fruiting perianthgreen . Prainea 1773.—TYPE: Fosberg. 1775, nom.cons.—TYPE: jaca Thunb. (= 37: 251.1776(‘ TYPE: section lis Cauliflori Cauliflori are cultivatedthroughout thetropics) . amplexicaul stipules;paleotropical indistribution(however, somespeciesof crowded butnotinlongitudinalrows; leavesalternateanddistichouswithlateralstipulesorspirally leaves alternateanddistichouswithlateralstipules;neotropical indistribution . Cauliflori 4. Leavesspirallyalternate;stipulesfullyamplexicaul,1cmorlonger, leavinganannulatestipulescar; 4. Leavesdistichous;stipuleslateralandnonamplexicaul,lessthan1cm,stipulescarnotannulate; (Parkinson)Fosberg). Artocarpus ). Inflorescences: unisexual,axillary orcauliflorous KingexHook.f.,Fl.Brit.India5:546.1888. Lour(= head enlarging atmaturity . . enlarging atmaturity . uniflorous ormultiflorous anddiscoid-capitate;fruiting perianthred, orange,paleyellow, orgreenish yellow) . Banks&Sol.exParkinson,J.Voy. SouthSeas45. A. anisophyllus 5. Inflorescences growth developdirectly from thetrunk orbranchesofprevious year’s . 5. Inflorescences alwaysaxillary Lour. Fl.Cochinch.546.1790.—TYPE: ), large fullyamplexicaulstipules(subg. Prainea scandens giving theinflorescence andsyncarpaspikyorbumpysurface . pistillate inflorescences withadjacentperianthsfusedonlymedially, leavingperianthapicesfree and . . smooth/uniform surface pistillate inflorescences withadjacentperianthsfusedapically, givingtheinflorescence andsyncarpa Thunb.,Kongl.SvenskaVetensk. Akad. Handl. Prainea ), achalazalthatisbasalrelative totheovary(not Batocarpus ) orsmalllateralstipules(subg. ) oralternateanddistichous(subg. Artocarpus: may havering-likeconstrictions(in (cauli- orramiflorous). Axillary inflorescneces mayalsobepresent andmaleinflorescences Artocarpus altilis Pseudojaca ), interfloral bractspresent orabsent. Staminate J.R.&G.Forst.,Char. Gen.Pl.:101,t.51, Artocarpus heterophyllus > Genera inthistribeare indigenoustothe n and 4 Rademachia incisa Renner, Bot.Jahrb.Syst.39:366.1907.— Rademachia × 4mm)( Jarrett 1959a , b , c,1960a; Berg ), alternateandspiral (subg. Cauliflori n and Prainea Asia eastward into Australasia and ). King. Clarisia (Parkinson)Fosberg). ) Leaves ). ’.TP: ’).—TYPE: Artocarpus altilis ) tocompletelyfusedone Thunb(= ), littletonoendosperm, Key totheGeneraandSubgeneraof Artocarpeae Prainea Lamarck). : simple(rarely com- Prainea Radermachia incisa A. annulatus Artocarpus alti- Pseudojaca ) monoecious ), (Parkinson) ) orpartially Artocarpus Artocarpus Artocarpus Pseudojaca Polyphema ) ...... ) and

1. cultivated throughout much ofthetropics. and tropics. and and South America) ( Fig. 1 ). Three species( Three species( Malesia inthesouth)eastward into Australasia, andOceania. Oceania) ortheNeotropics ( ate, rarely ellipsoid. Syncarp:cylindrical orellipsoid,rarely sparse orabsent. Staminateinflorescence: cylindricalorclav- caul, scarsannulate.Inflorescences: axillary, interfloralbracts ent, spongymesophyllcells loose. Stipules:large, amplexi- or pinnatified,hypodermispresent orabsent,resin cellspres- alternate andspiral,juvenile and adultleavesmaybeentire Artocarpus Artocarpus series description toaccommodatethe recircumscription toexclude where ( Jarrett 1959c ), andthis is anabbreviated and modified Artocarpus Artocarpus Genera— Distribution— Sbeu Subgenus Artocarpus Artocarpus Clarisia 1959.—TYPE: Artocarpus sect. Trécul, Ann. Sci.Nat.Bot.III,8:110. 1847. Arbor. 40:143.1959.—TYPE: 338. 1959.—TYPE: 1959.—TYPE: 137. 1959. 298. 1959.—TYPE: A. heterophyllus Cauliflori Jaca . e. ser. ser. e. ser. sect. Ruiz&Pavón. Artocarpus havebeenintroduced and ...... 4 ...... 3 . Artocarpus (Trécul) Renner, Bot.Jahrb.Syst.39:363.1907...... Artocarpus e. ser. Laevefolii . Leaves:simple(compoundin Angusticarpi A. altilis,camansi, Rugosi sb. subg. Duricarpus ...... Asia (Chinainthenorth,Indiawest, Artocarpus anisophyllus Artocarpus elasticus Incisifolii ) are cultivatedthroughout muchofthe F. M.Jarrett, J. Arnold Arbor. 40:343. J.R.&G.Forst., Artocarpus teysmannii Artocarpus altilis F. M.Jarrett, J. Arnold Arbor. 40:138. hasbeendescribedindetail else- Artocarpus e. ser...... 2 . F. M.Jarrett, J. Arnold Arbor. 40: F. M.Jarrett, J. Arnold Arbor. 40: F. M.Jarrett, J. Arnold Arbor. 40: 5 . Batocarpus Asperifolii flowers . s; nces Artocarpus rigidus Artocarpus Artocarpus and . . Artocarpus subgenusCauliflori Blume. Artocarpus Artocarpus F. M.Jarrett, J. Arnold (Parkinson)Fosberg. n and ...... Miq. A. heterophyllus Batocarpus A. altilis,A.camansi, subgenus subgenus Miq. Clarisia A. anisophyllus subgenus ug subg. Artocarpus Blume. Karsten, Central : Artocarpus Batocarpus Pseudojaca Clarisia Prainea ) are ) Jaca ),

Copyright (c) American Society for Plant Taxonomists. All rights reserved. Delivered by Ingenta to IP: 192.168.39.211 on: Fri, 24 Sep 2021 22:42:01 ~0.5 cmin A.sumatranus ate in shaped processes (free apicalportionofperianths):umbon- tranus fidus, A.pinnatisectus, of fourspeciesendemictothePhilippines( A. mariannensis has more recently included annensis three species( cies, Jarrett (1959c) treats asonehighlyvariablepantropical spe- the Moluccas( and differences, theyare treated asthree separatespecieshere. acuminate, whereas theyare rounded in A.sumatranus study doesnot includeallmembersoftheseries, butnonethe- from thewild tocultivatedformofbreadfruit. Thepresent altilis study, rough in upper surfaceoftheleavesissmoothin syncarp in compared to gene flow. phological differences thatsuggesttheyare notexperiencing maintained here duetoconsistent andeasilyrecognized mor- supported assister, buttheirstatusasseparatespeciesis and ~3.5cmin 7 SSEAI OAY [Volume 35 SYSTEMATIC BOTANY 2000 ). Among thoseassignedtosubgenus new specieshavebeendescribed( Jarrett 1975 ; Kochummen eral specieslevelcircumscriptions asdescribedbelow. (2006) and Jarrett (1959c) alsodiffered inthetreatment ofsev- eral oftheseries,wedonotrecognize themeither. Berg etal. did notmaintainthem.Duetothelackofmonophylyforsev- Jarrett’s sectionsandserieswithinsubgenus to thesubgenericrank. Berg etal.(2006) madereference to (1959c) intheexclusionofseries 31 speciesanddiffers from thatof Berg etal.(2006) and Jarrett or aerolate. subglobose; free perianthapiceseitherflexuous,indurated, 778 A.sumatranus taining cle characters)andgeographicaldistributionssupportmain- the changesbemaintained.Morphological(leafandpedun- its subspecieswere notsampled here, itisrecommended that culatus followed here. the present study, therefore Berg etal.’s(2006)treatment is known from onlyafewcollectionsandwere notincluded in A.elasticus neri scortechinii Rugosi, sented in endemic toBorneo,whereas therest ofthediversityrepre- Sre Series Since Jarrett’s (1959c,1960a)treatment of The circumscription ofsubgenus Berg etal.(2006) elevated Among thespeciesassignedtoJarret’s (1959c)series and A. maingayi , consideringthemalltorepresent arangeofvariation A. communis, wasnotincluded.Thethree specieshavedifferently to Berg etal.’s(2006)treatment differed asfollows: A. kemando Artocarpus elasticus ) andhybrids( Zerega etal.2005b ). Berg etal.(2006) A. brevipedunculatus. Artocarpus brevipedunculatus Incisifolii A. elasticus. A. jarrettiae A. melinoxylus A. brevipedunculatus. wasincludedin A. maingayi . Thesenewspeciesare endemictoBorneoand Artocarpus scortechinii A. scortechinii A. elasticus are larger andtheleafapicesof , andthelengthof malepedunclesvaries: were includedin A. altilis A. horridus , , are strongly supportedassister; A. multifidus, , ascircumscribed by Jarrett (1959c) , consists A. sumatranus buthasrecently beenrevised toinclude , truncate in Inthepresent study, were reduced by Berg etal.(2006) to and , between0.7and1.3cmin –breadfruit, isendemictoIndochina. , elongateprocesses are absentonthe andpresent in ), andthebreadfruit complexwhich A. treculianus and A. blancoi,horridus,camansi, A. elasticus A. melinoxylus and Atog Although . Additionally, theleavesof A. maingayi, hasgenerallysmallerparts A. scortechinii Cauliflori, A. kemando A. pinnatisectus Artocarpus A. camansi, A. maingayi. ), onespeciesnativeto ; and A. elasticus Artocarpus kemando A. melinoxylus A. blancoi,multi- subsp. Artocarpus whichiselevated A. scortechinii Artocarpus andconicalin . Inthepresent A. maingayi Artocarpus A. kemando ee includes here are strongly and Giventhese A. kemando, brevipedun- within , andthe A. suma- several , A. mari- , A. cor- and and and but are is A. A.

Artocarpusaltilis,A.camansi, quently pinnatifiedandpresence ofinflatedhairsonsyncarp. they allshare thefollowingcharacteristics:adultleavesfre- pled species( and Jarrett, ex Blume, genus syncarp. of adultpinnatifiedleaves,butlacktheinflatedhairson rate, well-supportedcladealsocharacterizedbythepresence breadfruit and clade (100%bootstrap)thatissistertoacontainingthe A.lowii Berg, Artocarpustreculianus lineage andBerg etal.’s(2006)changesare notmaintained. less indicatesthatseries ing westward toSriLanka ( Thailand, andtheNicobarIslands,withsomespeciesextend- Moluccas, NewGuinea,Malaya,Indonesia,Myanmar, the Malesianregion and isdistributedinthePhilippines, tained here tobepartofsubgenus ylus blancoi Artocarpusaltilis 2005b ). A.mariannensis lis and South America, andcoastalWest Africa. Indonesia, Malaysia,theCaribbeanIslands,tropical Central ics ( Zerega etal.2005b ), whereas A.camansi detailed inthediscussion, Given theproblematic positionandlackofstrong evidence the subgenusandthatlatterremains ofuncertainaffinity. present studyindicatesthattheformertwospeciesare partof India ( A.sepicanus A.nobilis The widelycultivatedspecies of Micronesia ( . 2. A.tamaran A.rigidus ing enormoussizes (upto100 A.annulatus dric toclavate(surfacewrinkled byring-likeconstrictionsin ent ( leaf axils,cauliflorous orramiflorous, interfloralbractspres- large amplexicaul,scarsannulate.Inflorescences: solitaryin resin cellsabsent,spongymesophyllcompact.Stipules: leaves entire, juvenileleavesmaybelobed,hypodermisand ated description.Leaves:simple,alternateandspiral,adult it iselevatedhere tothesubgenericrank,withanabbrevi- A.integer hasalsoundergone introgressive hybridizationwith Jarrett (1959c) notedthree anomalousspecieswithinsub- Distribution— Species— Sre Series Artocarpus Gagnep., A. treculianus nov. 40: 327.1959.—TYPE: A. annulatus A. camansi A. hirsutus (Elmer)Merr., Artocarpus King, A. horridus Thwaites, Artocarpus , free perianth apicesflexuous. Blume, Cauliflori Becc., andspreads intoOceaniaandthroughout thetrop- A. excelsus Diels, There are 31speciesincludedinthissubgenus: ). Syncarp:cylindrictoclavate orellipsoid,reach- A. maingayi A. pinnatisectus,horridus, subgenus Rugosi A. mariannensis A. multifidus inMicronesia ( Fosberg 1960 ; Zerega etal. Blanco, (Parkinson)Fosberg, A. teysmannii ), eastward intotheupliftedlimestoneislands : ugns Subgenus ) orabsent.Staminateinflorescence: cylin- Jarrett, maybemostcloselyalliedwiththe unsam- A. hirsutus,nobilis, A. sarawakensis wasdescribed by Jarrett (1959c) , and A. sericicarpus e. ser. A. obtusus Jarrett, cladesand and A. brevipedunculatus King, Cauliflori Incisifolii A. chaplasha Cauliflori A. kemando Artocarpus integer A. nobilis A. blancoi Jarrett, and A. sepicanus Artocarpus Miq.,and A. hirsutus A. mariannensis A. altilis ), andintothe Asian mainland. × Jarrett, 50cm)in Jarrett, F. M.Jarrett, J. Arnold Arbor. A. excelsus doesnotrepresent anatural A. mariannensis Jarrett, Artocarpus F M art) eea, stat. Zerega , Jarrett) M. (F. A. camansi Miq., ) andthewestern Ghatsof Roxb., formawell-supported A. odoratissimus wasdomesticatedfrom A. anisophyllus isconcentratedin A. pinnatisectus A. treculianus and Lamarck, A. sumatranus and ispresently main- A. scortechinii (F. M.Jarrett) C. A. heterophyllus A. lanceifolius . . A. elasticus Trécul, Artocarpus blancoi (Thunb.)Merr. A. sepicanus. . iscultivatedin A. multifidus Artocarpus alti- formasepa- A. hispidus A. melinox- Elmer. Miq., Blanco, Blanco, Reinw. Jarrett, Merr., Roxb., Roxb., King, King, The and ) as ) A.

Copyright (c) American Society for Plant Taxonomists. All rights reserved. Delivered by Ingenta to IP: 192.168.39.211 on: Fri, 24 Sep 2021 22:42:01 of because only“small” differences separated them.Descriptions P. frutescens two speciesof relationship further. additional charactersandall taxamayhelptosupportthis Prainea on chloroplast cent pistillateperianths.Previous phylogeneticstudiesbased Artocarpus indicates that above, of this positionandtheintermediacyofcharacters,asdescribed 779 ZEREGAET AL.:ARTOCARPUS medially fusedbutfree apically)withsubgenus and perianthfusioncharacters(adjacentpistillateperianths arrangement (spirallyarrangedwithamplexicaulstipules) subgenera 2010] is alliedwithsubgenus A.annulatus are notfoundintherest ofthegenus. Although affinities of marily bythepresence ofcauliflorous inflorescences, which A.annulatus (absent in phyll andtheabsenceofresin inthespongymesophyllcells indicates that perianths completelyfree from oneanother. rescence: globosetoshortobovoid. rescences: axillary, interfloralbractspresent. Staminateinflo- small, nonamplexicaul,scarslateralorintrapetiolar. Inflo- resin cellspresent, spongymesophyllcellsloose.Stipules: hous, juvenileandadultleavesentire, hypodermisabsent, to subgenericrankhere. Leaves: simple,alternateanddistic- Jarrett (1959b) resurrected ittogenericstatus.Itisreduced (1907) reduced ittosectionalstatuswithin the wildform as twovarieties, the Moluccas,andwesternNewGuinea.Ithasbeentreated and isthoughttobeindigenousSumatra,Borneo,Sulawesi, in Thailand,Malaysia,andpartsofIndonesiaMyanmar, Artocarpusinteger it iscultivatedthroughout muchofthetropics andsubtropics. specifically tothewesternGhatsofIndia( Wight 1843 ). Today to beindigenoustheIndiansubcontinentandpossiblymore placement of presence ofcauliflorous inflorescences, strongly supportsthe viously beensuggested,molecularevidence,aswellthe there isnobootstrapsupportforthisrelationship. However, 3 3. integer Artocarpusannulatus endemic toSarawak. Jarrett (1959b) and Berg etal.(2006) recognized fouror Subgenus This subgenusincludesthree speciesandisdefinedpri- The phylogeneticanalysisofmoleculardata presented here Prainea Distribution— Species— P. frutescens Artocarpus (= Jahrb. Syst.39:366.1907.—TYPE: 5: 546.1888. Motley, stat.nov. (Thunb.)Merr. within Artocarpus scandens wasoriginallydescribedby King (1888) . Renner Prainea thathaslosttheabilityforbelatedfusionof adja- A. heterophyllus Three speciesare includedinthissubgenus: into Artocarpus ). to Cauliflori A. annulatus Prainea and sb. subg. A. integer Prainea Prainea Artocarpus ndhF A. heterophyllus A. integer compared toothersubgeneraof Artocarpusheterophyllus (chempedak)isdistributedandcultivated Artocarpus P. scandens P. scandens Jarrett, and26SrDNA sequencesalsoplaced represents amonophyleticgroup within , respectively. Berg etal. (2006) reduced isnestedwithin appearstobeintermediatebetween Prainea n and Prainea var. Pseudojaca insubgenus ( Zerega etal.2005a ). Analysis of var. (King)Renner). and et sect. A. heterophyllus and silvestris Pseudojaca. King.inHook.f.,Fl.Brit.Ind. (King)Zerega, Supardi, and are basedonlimited material, integer, and A. integer, Prainea inhavingcompactmeso- P. papuana Syncarp A. integer . . acultivatedform,and Artocarpus annulatus Cauliflori Prainea scandens Itshares theleaf Artocarpus (jackfruit) isthought (King)Renner, Bot. notexaminedin : globose,adjacent Lamarck, and into Artocarpus havenotpre- . Artocarpus. although , Artocarpus P. limpato King and is A. It

4. uana Artocarpusfrutescens New Guinea. tion ismaintainedhere. and NewGuinea.Jarrett’s (1959b)specieslevelcircumscrip- uana evergreen forest inMalaya,Sumatra,andBorneowhile than thoseof ranges andtheinflorescences of ft. inBorneo). P. frutescens in lowlandevergreen forests to2,500ft.inMalaya,while and however, cies. Itisalso readily distinguishedby itslongpeduncles, Philipppines and doesnotoverlaprangeswith theotherspe- sister tooneanother. ties represent three distinctlineages,andthat theyare not lacucha cies, thepresent studyincluded species, thesechangesare notmaintained. Among thesespe- the phylogeneticanalysisofmolecular dataofsomethese morphological characters,biogeographicaldistributions,and var. ( nigrifolius, described from China( Artocarpus least apicallyandmediallytoadjacentperianthapices. ate. Syncarp:globoseorlobed,pistillateperianthsfusedat Staminate inflorescence: globose toobovoid,cylindricorclav- be onshortshootsorolderwood),interfloralbractsabundant. intrapetiolar. Inflorescences: axillary(orstaminateonesmay compact. Stipules:small,nonamplexicaul,scarslateralor hypodermis andresin cells absent,spongymesophyllcells alternate anddistichous,adultjuvenileleavesentire, Pseudojaca perianth apices.Jarrett’s (1960a) circumscription ofsubgenus leaf arrangementandcompletefusionofadjacentpistillate morphologically withinthegenus Artocarpus Artocarpus subgenus present study, however, theyallshare thetypicalcharactersof cus fretessii, A.ovatus, bined severalspecies,subspecies,andvarieties( remains untestedandunchanged. A. albobrunneus Species— Distribution— Since Jarrett’s (1959c,1960a)treatment, severalnew Subgenus Within subgenus Artocarpus ; Berg 2005 ). Noneofthesespecieswere includedinthe refractus Jarrett, J. Arnold Arbor. 41:83.1960.—TYPE: Bot. Jahrb.Syst.39:368.1907. III, 8:117. 1847. (Becc.)Renner, and isrestricted tolowlandevergreen forests intheMoluccas Smith. 41: 134.1960.—TYPE: 1960.—TYPE: lacucha P. scandens . Phylogeneticanalysesindicatethat thesethree enti- P. scandens isupheldwith abriefdescription.Leaves:simple, and speciesassignedtosubgenus et sect. ser. Pseudojaca Buch.–Ham. isrestricted tolowlandevergreen forests to200 There are fourspeciesincludedinthissubgenus: ) into Pseudojaca P. papuana Prainea limpato occupydifferent niches( subg. A. pithecogallus Clavati ; Berg etal.2006 ), andThailand( Glandulifolium Malay Peninsula,Sumatra,Borneo,and and A. lacucha Artocarpus hypargyreus Artocarpus Pseudojaca (Becc.)Renner, andtheircircumscription in isuniqueasaclimber, and F. M.Jarrett, J. Arnold Arbor. 41:130. Pseudojaca Artocarpus ovatus contains24speciesandisdefined A. vrieseanus A. gongshanensis,nanchuanensis, . . A. scandens Prainea limpato Artocarpus altissimus Buch.-Ham.However, basedon and et sect. Berg et al.(2006) recently com- ( Wu andChang1989 ), Borneo F. M.Jarrett, J. Arnold Arbor. P. limpato A. dadah,ovatus, P. papuana Artocarpus Trécul, Ann. Sci.Nat.Bot. Artocarpus Pseudojaca (King)Renner. var. A. limpato isfoundinlowland Pseudojaca is restricted tothe Hance. P. scandens are generallylarger papillosus, occupydifferent byitsdistichous e. ser. Téu) Renner, (Trécul) Miq., (Miq.)J. A. dadah, A. thailandi- P. frutescens Peltati ae been have Artocarpus Pseudojaca and isfound and A. pap- P. pap- F. M. A. v. A.

Copyright (c) American Society for Plant Taxonomists. All rights reserved. Delivered by Ingenta to IP: 192.168.39.211 on: Fri, 24 Sep 2021 22:42:01 Artocarpusn. 1902 ) and that cent inthelatter. syncarp, nearlyglabrous intheformeranddenselypubes- species are similar, differing onlyintheindumentumon strap) monophyleticgroup sisterto A.n. and are polyphyletic. described by Jarrett (1960a) were includedinthisanalysis dus ( Jarrett 1960a ), ortreated as“informalentities”within ( Trécul 1847 ; Beccari 1902 ), separatedintoseveralsubspecies in dus into subspecies.Ofthese,onlythesubspeciesof species. to theislandofBorneo,while warrant resurrection tospecificrank( A.n. area. Thecombined phylogenypresented here suggeststhat treated four“informalentities” of subsequently demotedby Jarrett (1960a) . Bergwere etal.(2006) atonetimeor another describedatthespecificrankand marily leafvenationcharacters. All subspeciesof eages. Theirmorphologicaldifferences are slightandare pri- (restricted toBorneo)appear torepresent twoseparatelin- syncarp beingfinelyribbedin be distinguishedfrom oneanotherbasedonthesurfaceof forests ofIndia,China,Bangladesh,andIndochina.Theycan of thelatterextendsnorthward andwestward into monsoon there intotheMalaypeninsulaandIndonesia,whilerange Myanmar, therangeofformerextendssouthward from ern China. this rangeandextendsnorthward upto Yunnan insouth- from SouthernChinato Thailand) and of (100% bootstrap)asamonophyleticgroup. Whiletheranges study (allfrom Malaysia)andtheyare strongly supported Miq., data from thefifthsubspecies( be treated asasinglevariablespecies.However, additional rubrovenius A.nanchuanensis hypargyreus Trécul, 8 SSEAI OAY [Volume 35 SYSTEMATIC BOTANY 1960a ). Three individualsof in thelengthofpedunclesandindumentum( Jarrett Jarrett 1960a ). Thevariationwithinthespeciesoccurschiefly multiple namesatdifferent timesbythesameauthor (see common andvariablespeciesthathasbeendescribedunder the pistillateinflorescence ( Jarrett 1960a ). 15–40 mminthestaminateinflorescence and40–80mmin 780 C. Berg, A.albobrunneus Solomon Islands,Philippines. Indochina, southernChina,Malaysia,Indonesia, Australasia, desirable before anyactionistaken. lotii rifolius Within subgenus Species— Distribution— A. dadah A. nitidus ( Berg etal. 2006 ). Fourofthefive were includedinthepresent study. Variation present Gagnep., A. ovatus subsp. subsp. A. fulvicortex C. Y. Wu, A. gongshanensis A. parva Warb., and Hance, A. tomentosulus There are 24speciesincludedinthissubgenus: hasbeenvariouslytreated asseparatespecies subsp. Artocarpus n. , , borneensis humilis A. pithecogallus A. dadah Berg, A. lacucha S.Chang,C.Tan, andZ. Y. Liu, India, SriLanka,Myanmar, Thailand, A. nitidus Artocarpus n. Gagnep.( Gagnepain 1926 ), respectively). , , A. lacucha A. subrotundifolius A. glaucus griffithii , and Pseudojaca A. altissimus Artocarpus nitidus , and formawell-supported (100%boot- S.K.Wu exC. Y. Wu &S.Chang, overlapinThailandandpossibly subsp. Jarrett, A. n Trécul, , and A. lacucha C. Y. Wu, Buch.-Ham., A. dadah Blume, sbp subsp. severalspeciesare divided . subsp. A n. A. dadah A. nitidus A. n. (Miq.)J.Smith, A. tonkinensis A. nitidus A. ovatus subsp. lingnannensis A. dadah A. humilis subsp. Elmer, were includedinthis betreated asseparate A. gomezianus borneensis A. reticulatus A. nitidus . Itisrecommended lingnanennensis subsp. A. n. Artocarpus dadah A. longifolius subsp. griffithii . Thesetwosub- intheMalesian Blanco, borneensis subsp. A. thailandicus Becc.( Beccari A. Chev. ex. isrestricted griffithii (extending subspecies nitidus A. nitidus overlaps Wall ex. Miq., A. dadah A. niti- A. pete- humilis A. nig- A. niti- could Becc., may and isa ) is ) A. A.

Sahagunia C. Explorers Club. 0073161, TheGarden Clubof America Award inTropical Botany, andThe by theLewisB. and Dorothy CullmanFoundation, NSFgrantDEB- KEP, LAE,MIN,NY, PTBG,SAN,SING,US.Thisresearch wasfunded and herbariaforaccesstospecimens: BRIT, CHIC,F, FTG, GH,GUAM, the manuscript.Finally, wewouldliketothankthefollowinginstitutions specimens andDNA samplesandtworeviewers forhelpfulcommentson W. Clement,N.Cordeiro, H.Ndangalasi,D.Ragone,andG.Weiblen for Lum, V. Novotny, L. Raulerson,and A. Rinehart.We wouldliketothank of C.Y. Chong, L. Y. Fah, A. Hussin, R. Kiapranis,KiewM.Kostka,S. Annocarpus B. Binnend. Gagnep., cus Batocarpuscostaricensis bose, adjacentpistillateperianthsfree from oneanother. rescence: spicatewithanabaxialsterilestrip.Syncarp:glo- axillary, interfloralbractspresent orabsent.Staminateinflo- amplexicaul, scarslateralorintrapetiolar. Inflorescences: hous, adultandjuvenileleavesentire. Stipules:small,non- with abriefdescription.Leaves:simple,alternateanddistic- Soaresia C.ilicifolila Clarisiabiflora the Guianas,Brazilian Amazon Basin,andeastern Brazil. America intoVenezuela, Colombia,Ecuador, Peru, Bolovia, another oruniflorous. capitate withadjacentpistillateperianthsfree from one inflorescence: spicatewithanabaxialsterilestrip.Syncarp: on leaflessshortshoots,interfloralbractspresent. Staminate caul, scarslateralorintrapetiolar. Inflorescences: axillaryor adult andjuvenileleavesentire. Stipules:small,nonamplexi- logenetic findings.Leaves:simple,alternateanddistichous, Aliteria Acanthinophyllum Acknowledgments. We maintainBerg’s (2001)circumscription of Species— Distribution— Species— Distribution— Berg’s (2001)circumscription of Clarisia (Ducke)Fosberg, and Batocarpus Sahaguniamexicana Naturvidensk. Math. Afh. 5(2):316.1851.—TYPE: racemosa cons., non 1922.—TYPE: Batocarpusorinocensis zonicus TYPE: C. H.Schultz-Bip.,1863,nom.conserv. (Asteraceae).— Pavón). Lanjouw &Rossberg). TYPE: ifolia TYPE: Pavón). Benoist,Bull.Mus.Hist.Nat.(Paris),2(1):163.1929.— Allemão, RevistaBrazil.1:210.1857,nom.rejic., non (Sprengel) Lanjouw&Rossberg). Liebmann,Kongel,DanskeVidensk. Selsk. A. vrieseanus (Sprengel) Lanjouw&Rossberg. Aliteria sagotii Ducke, Arch. Jard. Bot.RiodeJaniero 3:38. Acanthiniphyllum strepitans Soaresia nitida (Ducke)Fosberg). There are three speciesincludedinthisgenus: There are three speciesincludedinthisgenus: Ruiz&Pavón,Fl.Peruv. Chil.128.1794,nom. Ruiz&Pavón,typ.cons. Ruiz&Pavón, Clarisia Karsten,Fl.Columb.2:67.1863.—TYPE: Costa Ricato Amazonian Boliva. From southernMexicothrough Central Allemão, RevistaBrazil.1:368.1858.— Annocarpus amazonicus The authors are gratefulforthefieldassistance Abat, 1792,nom.rejic.; —TYPE: Miq.,and Standley&L.O.Williams, Liebmann(= Benoist(= Allemão (= Karsten. B. orinocensis C. racemosa A. xanthocarpus Clarisia ilicifolia Clarisia Clarisia racemosa Allemão (= Karsten. Clarisia biflora Ruiz&Pavón,and Ducke(= reflects ourphy- Teysm. and Clarisia ilic- B. amazoni- (Sprengel) Batocarpus Ruiz& Ruiz& B. ama- Clarisia

Copyright (c) American Society for Plant Taxonomists. All rights reserved. Delivered by Ingenta to IP: 192.168.39.211 on: Fri, 24 Sep 2021 22:42:01 Ceet W L ad . . ebe 09. Mrhlgcl vlto i the in evolution Morphological 2009. Weiblen . D. G. and L. W. Clement, Cre, . . 92. Te lsiiain f oaee. Moraceae. of classification The 1962. H. J. E. Corner, breadfruit, of pollination the and Nectar 1981. M. B. N. Brantjes, Cen, . H Sgwr , . aah , . oe , . . isn D G Higgins, G. D. Gibson, J. T. Lopez, R. Tadashi , K. Sugawara, H. R., Chenna, Dtye, . . n G D Wiln . 20 n h oii o te i: phy- fig: genus The the 1942. of R. F. origin Fosberg, the On 2004. Weiblen . D. G. and L. S. Datwyler, 2006. Jarrett . M. F. and Corner , H. J. E. C., C. Berg, of species new A 2005. C. C. Berg, 2001. C. C. Berg, Jret F M. 15b. Suis n in Studies 1959b. M. F. Jarrett, 1990. Barnett. C. L. and Holmgren , H. N. phylo- K., P. Holmgren, versus Congruence 2004. Sytsma . J. K. and Hall, C. J. Argentina . L., Tucuman , 2. A. ver. Hipp, Name) (No NONA 1999. P . Goloboff, Quelques 1926. F . Gagnepain, in Introgression 1960. R. F. Fosberg, Knai S, . oeoi A Sgua ad . uhdaadu . 1997. Subhadrabandhu. S. and Sugiura , A. Yonemori , K. S., Kanzaki, Jret F M. 17 h snap f of syncarp The 1976. M. F. Jarrett, Bcai O. 10 1902. O. Beccari, S. C. Wojciechowski , F. M. Porter , M. J. Sanderson, J. M. G., B. Baldwin, Br, . 97 eiin o Arcn oaee ecuig (excluding Moraceae African of Revisions 1977b. C. C. Berg, Jret F M. 15a. Suis n in Studies 1959a. M. F. Jarrett, Kcumn K M. 20 2000. M. K. Kochummen, 1888 . G. King, Jret F M. 17 or e new Four 1975. M. F. Jarrett, in Studies 1960b. M. F. Jarrett, Jret F M. 16a. Suis n in Studies 1960a. M. F. Jarrett, Br, . 97 h Csila, tie f h Mrca, eae and renamed Moraceae, the of tribe a Castilleae, The 1977a. C. C. Berg, transcribed internal the of utility Phylogenetic 1992. G. B. Baldwin, 00 ZRG TA. ROAPS 781 ZEREGAET AL.:ARTOCARPUS 2010] Kes W J, . . udc , . . imr L A Wet ad . . Janzen. H. D. and Wiegt , A. L. Zimmer , A. E. Wurdack , J. K. J., W. Kress, Jret F M. 15c. Suis n in Studies 1959c. M. F. Jarrett, mulberry family(Moraceae) . n J D Topo 03. Mlil sqec ainet ih the with alignment sequence Multiple 2003. Thompson. Clustal seriesofprograms . D. J. and Journal ofBotany Singapore altilis Blumea logenetic relationships ofMoraceaefrom than Ficus Neotropica Monograph7 ductions tothefamilyandFicuswithadditionscorrections toFlora de laSociétéBotaniqueFrance 101–113 . the BiologicalSocietyofWashington SystematicBiology genetic accuracy:revisiting theincongruence lengthdifference test . other Phylogenetic relationships betweenjackfruit, thebreadfruit andnine oeo nomenon . Cmbl , n M J Dngu 95. Te T rgo o ncer ribo- nuclear eny . of region ITS The 1995. somal DNA:avaluablesource ofevidenceonangiospermphylog- Donoghue. J. M. and Campbell, de Belgique Ficus, Musanga ieain siderations . 1: theherbariaofworld Hoe odn: L Reeve. L. London: Hooker . pN cpDNA . 320–340. sion of 73–139. Mrca). (Moraceae) . of 298–368. 113 –155, redefined duetotheexclusionoftypegenus Compositae . spacers ofnuclearribosomalDNA inplants:anexamplefrom the Omdee “Olmedieae” . n L G Sw . Kaa upr: Sbh oety eatet Forest Department, Forestry Sabah Lumpur : Kuala Research InstituteMalaysia,andSarawakForestry Saw Department . . G. L. and of theNationalAcademy ofSciencesUSA 2005 . Use ofDNA barcodes toidentifyflowering . in 187–212 Pp. of of Artocarpus Prainea Artocarpus Annals oftheMissouriBotanicalGarden (oaee (Moraceae). Artocarpus 0 531–533. 50: Parartocarpus Scientia Horticulturae 9 187–252. 19: . . Lie ainl ebru Nederland. Herbarium National Leiden: . 7 267–407. 47: Garden’s Bulletin,Singapore Artocarpus Journal oftheArnoldArboretum Nelle Foreste diBorneo Journal oftheArnoldArboretum Blumea Moreae, Artocarpeae,andDorstenia(Moraceae)withintro- ugns subgenus ugns subgenus Molecular PhylogeneticsandEvolution Tree floraofSabahandSarawak,Malaysia Acta BotanicaNeerlandica and 1 767–777. 91: spp.from RFLP analysisofanamplifiedregion of 3 81–89. 53: Acta BotanicaNeerlandica 2 409–410. 22: Myrianthus and . p 4 4 n in 546 – 547 Pp. . ieaue Cited Literature Artocarpus . Nw ok: Nw ok oaia Garden. Botanical York New York : New . Artocarpus Pseudojaca . Nw ok: Nw ok oaia Garden. Botanical York New York : New . Artocarpus Artocarpus Artocarpus Hullettia Artocarpus Batocarpus Artocarpus Nucleic AcidsResearch Artocarpus Artocarpus Systematic Botany 0 57–66. 70: 3 86–91. 73: Artocarpus Artocarpus ). ). Artocarpus Bulletin duJardinBotaniqueNational J.R.&G.Forster. nom.conserv . . Frne: Tp d S Landi. S. di Tip. Firenze : . 5 99–101. 55: . . . . . Journal oftheArnoldArboretum Journal oftheArnoldArboretum Journal oftheArnoldArboretum andalliedgenera,I.Generalcon- ovax ’noCie. d’Indo-Chine. nouveaux andalliedgenera,III. A revision andalliedgenera,IV. A revision as. Mrca). (Moraceae). Karst. andalliedgenera,II. A revision 4 35–39. 24: andalliedgenera,V. A revi- 0: 8369–8374. 102: Flora ofBritishIndia . 2: 73–82. 26: . speciesfrom Indo-Malesia (Moraceae)from Thailand . 0 30–37. 40: -aunique biologicalphe- n irnsa. Micronesia . in 2 247–277. 82: 0 1–29. 40: 0 345–352. 30: ndhF Moraceae -generaother 4 530–552. 34: sqecs. sequences. The Garden’s Bulletin 1 3497–3500. 31: : 3–16. 1: Index Herbariorum Olmedia , d , Soepadmo E, ed. , Proceedings of Brittonia Proceedings Artocarpus , d . D. J. ed. , from the Dorstenia, American Bulletin 61: 41: 12: 40: Wgt R. 14 1843. R. Java– Wight, from plants some of biology flower the On Artocarpées. 1953 . des L. Pijl, famille der la Van sur Mémoire 1847. A. Trécul, for primers Universal 1991. Bouvet. J. and Pautou G. Gielly , L. P., Taberlet, Nxn K C. 19–02. Wnld vr 100. taa, Nw ok: Published York : New Ithaca, 1.0000. ver. WinClada 1999–2002. C. K. Nixon, Ssm, . . J Mrwt , . . ie , . eoref E Cni M Sjhra, M. Conti, E. Nepokroeff , M. Pires , C. J. parsimony Morawetz, using J. J., analysis K. phylogenetic Systma, PAUP*: 2002. L. D. Swofford, anal- DNA Ribosomal 1997. Cozzolino. S. and Caputo, P. G., 1963. G. Siniscalco, Katyal. L. S. on and investigations Krishnamurthi, S. anatomical S., and Singh, Morphological 1965. R. M. Sharma, consen- and Congruence 1997. Wendel . F. J. and Schnabel, A. T., Seelanan, Nxn K C. 19 h prioy ace, nw ehd o rpd parsi- rapid for method new a ratchet, parsimony The 1999. C. K. Nixon, phy- molecular A 1994. Starr . M. E. and Schuette, P. K. L., D. Nickrent, Ski S, . ao ad . aaau . 20 2000. Nagamasu. H. and Kato, M. S., Sakai, Mnu, . 95. Foa otgn o te akri, jackfruit, the of ontogeny Floral 1985. W . M. Moncur, Ski S. 20 his olnto i adoieiu androdioecious in pollination Thrips 2001. S. and Sakai, Machado, A. C. Salamin, N. Cook, M. J. Weiblen , D. G. N., Rønsted, in 438–453 Pp. Moraceae. 1993. G. J. Rohwer, Artocarpeen der Systematik 2.0a7b. und version Anatomie zur editor, Beiträge 1907. alignment O. Renner, Sequence Se-Al. 2001. A. Rambaut, 1983. B. R. Primack, averaging model and selection Model 2004. Buckley . R. T. and D. Posada, Zrg, . . . D Rgn , n T J Mte 04 ope oiis of origins Complex 2004b. Motley . J. T. and Ragone, D. C., J. N. Zerega, Pollination 2004a. Weiblen . D. G. and Mound, A. L. C., J. N. Zerega, Mms, . A Htd , . aak , n T Ioe . 19 olnto biol- Pollination 1998. Inoue. T. and Yamaoka , R. Hatada, A. K., Momose, Psd, . n K A Cadl 98. Mdlet tsig h mdl f DNA of model the testing Modeltest: 1998. Crandall. A. K. and D. Posada, Zrg, . . . S Mr , . idvs , . hn , n T J Mte 2002 . Motley . J. T. Moracearum and Zheng, nonnulla Q. nova Lindqvist, C. Taxa Mori, 1989. S. C., Chang. J. N. S. Zerega, S. and Y. C. Wu, Oioo M C. 14 ntm ad itlg o pnape inflorescence pineapple of histology and Anatomy 1948. C. M. Okimoto, 77–99. Typhonium, Gnetum,Arisaema with generalremarks on fly-traps(speciesof Sciences Naturelles Molecular Biology amplification ofthree non-coding regions ofchloroplast DNA . sequences . foresnic interests . . . al ad . . hs 02. Utcla rsd: circumscription, : Urticalean 2002 . Chase. W. rosid ancestry, andphylogeneticsbasedon M. and Hall, C. J. (*and othermethods),version4 . Sunderland : Sinauer Associates . ysis asatoolfortheidentificationof New Delhi : Indian Councilfor Agricultural Research . Artocarpus sus inthecottontribe(Malvaceae) . mony analysis . 1149 –1160 . internal transcribedspacersequences . logeny of 8: 1527–1534. 88: ugs. fungus . midge pollinationmutualismmediatedbyamale-flowerparastic lus (Moraceae) inaseasonaltropical forest . fig-wasp the in co-divergence of symbiosis . years million 60 2005. Savolainen. V. Springer-Verlag . vascular plants 319–448. Jahrbücher fürSystematik,PflanzengeschichteundPflanzengeographie und Conocephaleen,insbesondere derGattung Oxford, U.K. : Department ofZoology, Oxford University . Malaysia. Sarawak, Department, Forest over likelihoodrationtests . in phylogenetics:advantagesofthe AIC andBayesianapproaches migrations inOceania . breadfruit ( 1017 –1026. (Thysanoptera: Thripidae) . mediated byanewspeciesofthrips, in theNewGuineaendemic ogy ofthegenus usiuin. substitution . black cohosh( Using amplifiedfragmentlengthpolymorphisms(AFLP)toidentify Sinensium . and fruit . by theauthor . Lam.(Moraceae) . American JournalofBotany Arceuthobium Botanical Gazette(Chicago,Ill.) Forst.III.Theflower . Icones PlantarumIndiaeOrientalis Proceedings. BiologicalSciences American JournalofBotany Acta BotanicaYunnanica Artocarpus altilis Bioinformatics . d . uizi J G Rhe , n V Btrc Berlin: Bittrich. V. and Rohwer , G. J. Kubitzki, K. ed. . Actaea racemosa Cladistics Forester’s guidetotheMoraceaeofSarawak 7 1105 –1109 . 17: Artocarpus : 38–157. 3: Science &Justice Australian JournalofBotany (Viscaceae) basedonnuclearribosomalDNA American Journalof Botany 5 407–414. 15: 4 817–818. 14: Mrca Moraceae. , International JournalofPlantSciences Systematic Biology , Moraceae):Implicationsfor human ). ). and Economic Botany Phytomorphology Antiaropsis decipiens 7 171–174. 37: 7 440–445. 87: 1 24–34. 11: Systematic Botany Abroma 9 1531–1546. 89: Cannabis sativa American JournalofBotany 1: 217–231. 110: Tropics 7: 2593–2599. 272: Thrips antiaropsidis Artocarpus American JournalofBotany . Mda . . Pharoah. B. J. Madras: . The familiesandgeneraof ). ). 3 793–808. 53: rbcL, trnL-F : 165–172. 7: Annales Bogorienses 6 154–164. 56: Artocarpus heterophyl- Fruit culture inIndia 3 585–593. 33: Annona, Artocarpus, 5 185–201. 15: 1 760–766. 91: Ficus (Moraceae)-gall L.specimensof 2 259–290. 22: (Moraceae)is Castilla elastica . Annales des , and . Sarawak: . Botanische sp.nov. Plant ndhF 165: 165: 81: 39: 1: .

Copyright (c) American Society for Plant Taxonomists. All rights reserved. Delivered by Ingenta to IP: 192.168.39.211 on: Fri, 24 Sep 2021 22:42:01 GenBank accessionnumbers(ITS, mation [collectionlocality, collectionnumber(herbariumcode)],and specimen, thefollowingislisted:sampledtaxa,voucherspecimeninfor- abbreviations followIndexHerbariorum ( Holmgren etal. 1990 ). Foreach MORACEAE: rather thanleafmaterialdriedonsilica,isindicatedbytwoasterisks. are indicatedbyanasterisk.Materialacquired from herbariumsamples, Previously publishedsequencesdownloadedforinclusioninouranalyses spe- and Systematics 2005b. Motley . J. T. and Ragone, D. C., J. N. Zerega, 8 SSEAI OAY [Volume 35 SYSTEMATIC BOTANY Weiblen . D. G. and Datwyler , L. S. Clement, L. W. C., J. N. Zerega, 782 Appendix 603–615. cies limitsofbreadfruit ( Mrca). (Moraceae) . 2005a . Biogeography anddivergence timesinthemulberryfamily FJ917103. heterophyllus Malaysia, FJ917096. N.Zerega 228 (NY), FJ917017,FJ917081. ticus FJ917098; FJ917050,FJ917111; FJ917051,FJ917112. N.Zerega 69 FJ917021, FJ917085. Artocarpusblancoi annulatus Miq., Singapore, Roxb., India, Ragone 236 dadah 257 FJ917041, FJ917105. Fiji, FJ917116; MarianaIslands, altilis Weiblen 1233 FJ917053, FJ917114. Malaysia, Hawaii, U.S. A., Artocarpusnitidus sis N.Zerega 233 (CHIC), FJ917033,FJ917097. Vives s.n. Artocarpusinteger hispidus Zerega 13 Florida, U.S. A., Trécul, Rota,CNMI, (CHIC),FJ917043,FJ917107. D. Ragone486 Reinw. ExBlume,Malaysia, (Parkinson)Fosberg, Samoa, Miq.,Malaysia, 1. Specimens usedinthephylogeneticanalyses. Herbarium Jarrett, Malaysia, (NY),FJ917052,FJ917113. Antiaropsis decipiens (NY),FJ917018,FJ917082. Artocarpusexcelsus ** Jarrett, Sarawak, Artocarpusheterophyllus N. Zerega 263 N. Zerega 256 (PTBG),FJ917023,FJ917087. Molecular PhylogeneticsandEvolution (MIN), AY730142* ( Rønsted etal.2005 ), —. (CHIC),FJ917015,FJ917079. (NY),FJ917024,FJ917088. (CHIC),FJ917030,FJ917094. Lamarck, Singapore, Huq andMia10274 N. Zerega 210 Fisher 96–58 N. Zerega 4 (PTBG),FJ917057,FJ917118; SocietyIslands, (Thunb.)Merr., Malaysia, Artocarpuscamansi ** (Elmer)Merr., Philippines, Artocarpuslowii Trécul subsp. Artocarpuskemando N. Zerega 245,247, Artocarpus (CHIC),FJ917040,FJ917104. N.Zerega 162 and N. Zerega 258 D. Ragone311 Artocarpusfulvicortex (CHIC),FJ917027,FJ917091. (FTG),FJ917016,FJ917080. (NY),FJ917035,FJ917099. Artocarpusmaingayi trnL-F ** Jarrett, Sabah, R. Primack38722 K.Schum.,PapuaNewGuinea, 241 (BRIT),FJ917047,—. Mrca). Moraceae). , N. Zerega 243 D. Ragone453 Artocarpuslakoocha

Lamarck, Hawaii,U.S. A., ); —=sequencenotobtained. (CHIC),FJ917042,FJ917106; Artocarpuslanceifolius Artocarpushirsutus Zerega 219 King,Malaysia, lingnanensis (CHIC),FJ917022,FJ917086. (CHIC),FJ917031,FJ917095. Blanco,PapuaNewGuinea, (PTBG),FJ917056.FJ917056; Artocarpusglaucus and Miq.,Malaysia, Artocarpusanisophyllus Artocarpuschaplasha Artocarpusmariannen- N. Zerega 227 250 (CHIC), Systematic Botany (GH),FJ917046,—. J. Beamanetal.7918 7 402–416. 37: (CHIC),FJ917039, (CHIC),FJ917032, (PTBG),FJ917055, Jarrett, Malaysia, Ramos s.n. (Merr.) Jarrett, Artocarpuselas- King,Malaysia, N. Zerega 246 Artocarpus Artocarpus Artocarpus Artocarpus Artocarpus Artocarpus Lamarck, FJ917034, * Roxb., ** N. Zerega (CHIC), Blume, Roxb., (NY), 30: D. N. G. **

CANNABACEAE: FJ917078. ovatus Singapore, mus N.Zerega 262 Artocarpusnitidus FJ917092; Malaysia, griffithii 270 N.Zerega 205 nitidus teatus U. S. A., (NY), FJ917011, FJ917075. FJ917070. Hullettiadumosa carica Watson, CostaRica, FJ917049, FJ917110. enii N.Zerega 248 Artocarpussepicanus Weiblen 1460 FJ917073; FJ917048,FJ917109. ex Heyne,Nutt.,Malaysia, Weiblen 1428 Guinea, Philippines, (MIN), FJ917010,FJ917074. (MIN), FJ916997,FJ917062. FJ917064. Sorocea briquetii bachii Artocarpustonkinensis Artocarpustamaran tundifolius (MIN), FJ916996,FJ917061. Brosimum lactescens L. O.Williams, Peru, (MIN), FJ917001,FJ917066. Bagassaguiannensis Papua NewGuinea, Zerega 203 9700 FJ917005, —. —. FJ917012, FJ917076. F059 (Ssm e a. 2002). al. et (Systma AF501599* et al.1997 ), —. (CHIC),FJ917036,FJ917100. Treculia africana King,Singapore, Blanco,Malaysia, (US),FJ917004,FJ917069. L.,New York, U.S. A., C.Berg, Peru, ** (King)Becc.,PapuaNewGuinea, Blanco,Hawaii,U.S. A., Trécul subsp. (King)Jarrett, Singapore, N. Zerega 16 N. Zerega 61 Maclurapomifera Sparattosycedioica (CHIC),FJ917020,FJ917084. Artocarpuspetelotii ** Elmer, Philippines, N. Zerega 224 (MIN), AY635565*, —. Burley 69 (MIN),FJ917002,FJ917067. (CHIC),FJ916993,FJ917058. Treculia obovoidea (CHIC),FJ917037,FJ917101. Cannabis sativa (CHIC),FJ917026,FJ917090. Humuluslupulus J.F. Macbr., Peru, King,Malaysia, Trécul subsp. Poulseniaarmata G. Weiblen 1417 Artocarpustreculianus Decne.,Tanzania, (NY),FJ917003,FJ917068. Becc.,Singapore, (SING),FJ917019,FJ917083. (S.Moore) C.Berg, Peru, borneensis Aubl N. Zerega 226 (NY),FJ917013,FJ917077. Diels,PapuaNewGuinea, G. Weiblen 1229 ** A. Chev. Ex.Gagnep.,China, (NY),FJ917008,FJ917072. G. Weiblen 1463 N. Zerega 218 N. Zerega 261 G. Weiblen 1501 (CHIC),FJ917054,FJ917115. N. Zerega 249 ., G.D.Weiblen 1677, (Raf.)C.K.Schneid.,New York, U. S. A., Castillaelastica Artocarpusrigidus Clarisiabiflora Batocarpuscostaricensis N. Zerega 15 Bur., AY730141* ( Rønsted etal.2005 ), Praineapapuana L., Y18150* and Y12587* ( Siniscalco ** Gagnep.,China, Artocarpussericicarpus (Merr.) Jarrett, Singapore, ** N.E.Br., Cameroon, L.,DQ005990*( Kress etal.2005 ), Artocarpusnitidus Madulid 6810 humilis N. Zerega 202 (MIN),FJ916995,FJ917060. G. Weiblen 1457 N. Zerega 242 N. Zerega 216 Prainealimpato (CHIC),FJ917038,FJ917102. (Miq.)Standley, Panama, (CHIC),FJ917029,FJ917093. (CHIC),FJ917025,FJ917089; (MIN),FJ917044,FJ917108. (MIN),FJ917000,FJ917065. Ndangalasi andCordeiro 7 Artocarpusvrieseanus (MIN),FJ916998,FJ917063. and (NY),FJ916994,FJ917059. Morusalba (Becc.)Jarrett, Malaysia, Dorsteniachoconiana Elmer, Hawaii,U.S. A., Artocarpusodoratissi- W. Takeuchi 1518 Ruiz&Pav., Peru, Sessé, 264 Artocarpusscortech- (GH),FJ917045,—. Parartocarpusbrac- Blume,Malaysia, Becc.,PapuaNew (CHIC),FJ917014, (CHIC),FJ917006, (CHIC),FJ917028, (CHIC),FJ917009, Artocarpussubro- (MIN),FJ916999, Hsiu-Lan Ho757 French Guiana G. Weiblen 1701 G. Weiblen 1473 G. Weiblen 1238 (Miq.)Beumée Sorocea stein- Trécul subsp. Gillis 10954

L.,New York, Standley& Leeuwenberg Artocarpus * Jarrett, ** N. Zerega (GH), Miq., Ficus G.D. (F), (S), (S), S. G.