Copyright (c) American Society for Taxonomists. All rights reserved. Delivered by Ingenta to IP: 192.168.39.211 on: Fri, 01 Oct 2021 12:59:15 without periderm, andwithpale-green rotate corollas. This marily herbaceous plantswithlittleornosecondary growth, U. S. A. toBolivia( Mione and Yacher 2005 ). Theseare pri- includes about10speciesdistributed from thesouthwestern belonged with that speciespreviously assignedto DOI 10.1600/036364411X553243 © Copyright2011 bythe American SocietyofPlantTaxonomists Systematic Botany of of ,thenassumedto beamongtheclosestrelatives sampled, alongwithrepresentatives ofseveralothergenera cpDNA restriction siteanalysis,inwhich14specieswere basis ofmorphology( Mione and Anderson 1996 ) anda locations inthe Andes ofSouth America. endemics andfoundinremote, historicallyunder-collected come tolightonlyrecently becausemanyspeciesare narrow 2000b, and floralmorphology;muchofthischaracterdiversityhas 2000a, 2008). 1993, al. 2007, et Mione 2004, 2008; 2007b, 2007a, 1998, al. et 1994 ), aswellthediscoveryofmanynewspecies.( Leiva G. reassigned to to different genera(e.g. derives from boththerecognition ofseveralspeciesassigned D’Arcy 1991 ). Theexpandeddiversityrecognized atpresent thought (e.g.fourspeciesin D’Arcy 1979 and10speciesin hummingbirds (Mioneand LeivaG.,fieldobservation). species are visitedbybees ( Eickwort 1967 ; Williams 1985 ) and lination hasnotbeenstudiedextensively, although Buchmann 1983 ; Knapp 1986 ; Sazima etal.1993 ); tion bypollinators. in floralcharactersare expected tobecausallyrelated toselec- and possessesantherswithterminalpores. Thesedifferences tudinal antherdehiscencewhereas cally distinct: approximately 1,500species. Thetwogeneraare morphologi- Jaltomata tribe Solaneae( Olmstead etal.2008 ). With about60species, Olmstead etal.2008 ); thetwogeneratogethercomprise et al.1999 ; Hu andSaedler2007 ter group to ; Weese andBohs2007 ; Two subgroups of Jaltomata identify studies phylogenetic Molecular Jaltomata to pollination. tion betweenred nectarproduction andcampanulatefloralforminmultiplelineages,suggestingacommonevolutionarysyndrome similar tomanyspeciesof character statereconstruction supportsaviewofthecommonancestorgenusoriginatinginSouth America andhaving rota cal diversity. We alsoidentifyanearly-diverging lineageof western South America, characterizedbyorangefruits, andaprimarilyMesoamericancladewithblack/purplefruit andlittlemo mately 60speciesfrom CentralandSouth America. Phylogeneticanalysesidentifytwoprimarygroups: amorphologicallydiverse Keywords— Abstract— isamuchsmallercladethan isamuchmore diversegroup thanpreviously ( Mione etal.1994 ). The latterstudyalsoshowed (2011), 36(1):pp.153–162 1 Department ofBiology, UniversityofWashington, Box355325,Seattle,Washington 98915-5325U.S. A. Solanum Sister Genusto Clr y ubr: ula Gn Pyoey f of Phylogeny Gene Nuclear Numbers: by Color Jaltomata Jaltomata Jaltomata DNA sequencesfrom thenucleargene

2 Department ofBiology, CentralConnecticutStateUniversity, 1615StanleyStreet, NewBritain, BS oeua sseais, ncer N hlgn phylogeny , DNA, nuclear systematics, molecular GBSSI, Jaltomata Solanum yn . Miller , J. Ryan ( Olmstead andPalmer1992 ; Olmstead Jaltomata produces floralnectarandhaslongi- ( Hunziker 1979 ; Mione etal.1993 , . Theblack/purple-fruited subgroup Saracha Solanum isbee-pollinated( Eickwort 1967 ; exhibitsanarrayofvegetative havebeenrecognized on the ) andallof . Inaddition,weinferindependentcolonizationsoflomashabitatsby Solanum Solanum

3 1 Solanum Author forcorrespondence (email:[email protected]) Toa Mione, Thomas Hebecladus Jaltomata lacksfloralnectar Hebecladus , whichincludes omnctn Eio: a Potter Dan Editor: Communicating , SupportsThreeCladesDiffering inFruitColor Connecticut 06050-4010U.S. A. and Jaltomata waxy asthesis- Jaltomata were usedtoassessphylogeneticrelationships within Saracha Jaltomata being 2 , pol- 3 Hn-a Phan, Hanh-La

specieswithred fruits, whichissistertotherest ofthegenus. Ancestral 153 waxy subgroup includestwowidespread species( and anew, undescribed species( corolla formandcolorvary markedly. Two species, spicuous periderm,butafeware herbaceous.Inthisgroup, ( Islands ( D’Arcy 1982a to Bolivia,thedesertalongcoastofPeru, theGalápagos , 1982b about 50speciesdistributedinthe Andes from Venezuela ), andtheGreater Antilles tributed speciesofMexicoandCentral America. and westernSouth America, andabouteightnarrowly dis- J.repandidentata species sampled,only endemic tothathabitat( Rundel etal.1991 ). Ofthefour lomas east ( Dillon 1997 , 2005 ert andare separatedfrom themuchhigher Andes tothe ). Manyspeciesthatliveinlomasare ties. Theseare virtualislandssurrounded byhyperariddes- and rocks creating verdant oasesknownaslomascommuni- slopes andmountaintops,moisture dripsoff thevegetation ocean fog( Rundel etal.1991 ). Where foghitsthenear-shore tains andslopesare highenoughtobebathedseasonallyin places where coastaldesertsare punctuatedbysmallmoun- tinctive areas occurfrom northernPeru tonorthernChile,in grow inuniquedesert-fogareas knownaslomas.Thesedis- (e.g. Mione etal.2001 ). orange nectaratleastonce,eitherinthefieldorcultivation producing clearnectarhave beenobservedproducing red/ ( Mione and Anderson 1996 ). Three otherspeciesnormally but occursin13speciesof the stamens,onwhichred/orange nectarpools. sess abowl-likefloralstructure, formed bythefusedbasesof study), share auniquestigma andstylemorphologypos- lshl 93; Da 17 ilas 95; Dvs 96; Schultes 1986 ; Davis 1985; Williams 1976; Díaz 1973 ; ( Altschul eggplant), fruits ofmost tant genusofSolanaceae(including tomatoes,potatoes,and onization ofthelomasbydifferent Andean progenitors. differences inleafdeciduousness supportahypothesisofcol- the Andes. Diversecorolla forms,nectarcolorvariation, and J. antillana In contrast,thered/orange-fruited subgroup includes At leastsix Red nectarcolorisexceedinglyrare ( Hansen etal.2007 ), Wie While . Solanum 1 n ihr G Olmstead G. Richard and ; Mione 1992 ). Theseare mostlyshrubs withacon- Jaltomata Jaltomata ) ofsouthernNorth America, Central America, isthe largest andmosteconomically impor- species,includingtwowithred nectar, J. aspera Jaltomata Jaltomata (), Jaltomata occursinboththelomasand Jaltomata speciesandshowacorrela- speciesalsoare consumed J . “hummingbird” inthis from Peru andBolivia , agroup ofapproxi- 1

J. procumbens group from te corollas rphologi- related J. aspera and

Copyright (c) American Society for Plant Taxonomists. All rights reserved. Delivered by Ingenta to IP: 192.168.39.211 on: Fri, 01 Oct 2021 12:59:15 Massachusets). Parsimony-informative gapswere codedaspresence/ the program MacClade4.08OSX(Sinauer Associates, Inc, Sunderland, TreeBASE (studynumberS10388). in Appendix 1,andthealigneddatasetwithgapcodes isdepositedin ited inGenBankunderaccessionnumbers GU256289-GU256358aslisted Codes Corp., Ann Arbor, Michigan). Generatedsequenceswere depos- proofed, edited,andcontigsassembledusingSequencher v.4.7 (Gene and fourtosixcloneswere sequencedforeachtaxon.Sequence datawere the TOPO TA cloningkitforsequencing(Invitrogen, Carlsbad,California), polymorphism wasdetectedduringdirect sequencingwere clonedusing ing ( Yuan etal.2006 ; TablePreviously designedprimers forSolanaceaewere alsousedforsequenc- 1 ). Amplification products forwhichlength X58453) and sequencing were designed from previously published ers. cycle sequencingkitson ABI model377or3100automatedDNA sequenc- BigDye Terminator v3.1(AppliedBiosystemsInc,FosterCity, California) DYEnamic ETTerminator (GEHealthcare, Piscataway, New Jersey) or prior tosequencing.Bothstrandswere directly sequencedusingeither polyethylene glycol8000/NaClsolutionandwashedwith70%EtOH Amplified temperatures of50–55°C using primers2F, 13R1and13R2from Table 1 waxy . Granule BoundStarch SynthaseI(GBSSIgene,commonlyreferred toas was performedtoamplifytheregion spanningexons2–13ofthegenefor (Promega, Madison,Wisconsin). Thepolymerasechainreaction (PCR) ( Doyle and1987 collected, silica-geldriedtissueusingthemodified2×CTAB method ) andpurifiedusingWizard minicolumns and Bohs2007 ). and sister cladetoSolaneae( Olmstead etal. 2008 ), and Witheringia solanacea (Appendix 1).Fivespecieswere selectedasoutgroups: taxa, includingeightnewandunnamedwere includedinthisstudy [Volume 36 SYSTEMATIC BOTANY Bye 1996 ), anunnamedraceof some, butnotall,collectionsof fruited subgroups of known from boththered/orange-fruited andblack/purple- green, toorangeorred atmaturity. Green-fruited speciesare The fruits are round, fleshyberriesrangingfrom purple,black, and Raffauf 1990 ; Laferrière etal.1991 ; Mione andBye1996 ). 154 infer theevolutionofmorphologicaltraitswithin within thegenusidentifiedbyprevious studiesand2)to tives were: 1)totestthevalidityoftwomainsubgroups in itssistergroup, relatively more uniformflowertypesandabsence ofnectar tube lengthandnectarcolor, within Jaltomata J.“ represented inthisstudyas colored nectarproduction, fruit color, habitat,andhabit. structions tofocusontheevolutionoffivetraits:floralshape, 2007 ; Spooner etal.2008 ). We theninferancestralstaterecon- ( Peralta andSpooner2001 ; Levin etal.2006 ; the utilityofusing Weese andBohs within gene waschosenforthisstudybasedonphylogeneticstudies levels ofdivergence ( Sang 2002 ; Hughes etal.2006 ). The resolve phylogeneticrelationships whencpDNA exhibitslow waxy of divergence betweenspecies.Lowcopynucleargeneslike lished cpDNA genesequencesfor Pyoeei Analyses— Phylogenetic Mlclr Techniques— Molecular aa Collection— Data The lackofaphylogenyforthemajorityspecies We focusonanucleargene,becausepreviously pub- hummingbird.” Jaltomata S. melongena ). Amplifications were conductedin25µL volumeswithannealing havebeenusedsuccessfullyattheinterspecificlevelto Solanum andtheextensivefloraldiversity, especiallyincorolla waxy specificPCRprimers andinternalprimers( Table 1 ) usedfor Jaltomata products were cleanedbyprecipitation from a20% torepresent eachofthetwolarge , thesistergenusto , , aeil ad Methods and Materials Lycianthes heteroclita A totalof68accessionsrepresenting 50 Solanum sequences(DQ169009, AY996374, AY875405). waxy Jaltomata Total genomicDNA wasextractedfrom field- Sequences were manuallyalignedusing forresolving speciesrelationships , prompted thisstudy. Ourobjec- J . Green fruits are produced by . “green fruit,” J. procumbens J. chihuahensis tosamplethe diversityfrom the Jaltomata Jaltomata Jaltomata Solanum Solanum lycopersicum , incontrasttothe , whichindicated showlowlevels Solanum (Wlim 1985) (Williams J. lezamae Physalis alkekengi (Moe and (Mione clades( Weese Jaltomata (AP009280, Jaltomata , and , waxy . ,

at 0.5,reduced 20timestoaminimumof0.01).To verifyconvergence, branches evaluatedforeachtaxon,branch-lengthoptimizationstarted erogeneity, startingtrees created bystepwise-additionwith50attachment four categoriesofdiscrete approximation ofgamma-distributed ratehet- CIPRES cluster( Miller etal.2009 ) underdefaultparameters(including GARLI version0.96b( Zwickl 2006 ). Fortysearches were performedonthe ( Posada andCrandall1998 ). both the Akaike information criterionandBayesianinformationcritertion the data.Thesamemodelwassupportedasbest-fitinModeltest3.7by ( Yang 1994 ) modelofsequenceevolutionwasindicatedasthebest-fitto ( Hasegawa etal.1985 ) withdiscrete gammadistributedratevariation used todeterminethebest-fitmodelofsequenceevolution.TheHKY and Bayesianinference methods.DT-Model Select( Minin etal.2003 ) was was sequence one only 2), Table included inourphylogeneticanalyses. in (summarized sequences identical had 2000 ; Graham etal.2000 ). Whenmultipleaccessionsof the sametaxon absence charactersusingsimplegapcoding( Simmons andOchoterena ay1R (J) CA waxy_13R2 (J) waxy_12R (J) waxy_11R (J) CA waxy_11F (J) waxy_10R (J) GCA waxy_10F A waxy_8R waxy_8F (J) waxy_7R waxy_7F waxy_5R waxy_5F waxy_13R1 waxy_2F (J) –primersdesignedspecificallyfor J.sinuosa J.sanchez-vegae J.salpoensis J.repandidentata J.procumbens J.dentata J.bicolor appears inthephylogenetictrees are listed. cies, GenBanknumber, collectionlocality, andaccessionnumberwhich final analysesthatwere identicaltothelistedGenBankaccessions:spe- gene. To simplifythephylogenetictrees, taxawere removed from the cies, somewere identicalinDNA sequenceforexons2–12ofthe Maximum likelihood(ML)analyseswere performedusingtheprogram Phylogenetic analyseswere performedusingmaximumlikelihood Table Table name Species

. 2. When numerous collectionswere sampledwithinonespe- . 1.

(J) (J)

Jaltomata

TCTCCCATTTCTTGGCAGGTTC AGTGTCAACAAGTCCACCAGTC Y GAGTCAGGTGCCAATCTGTGC AACAGCTTGAAGTGTTGTATCCTGAC ACTCTTGTGTATCCATGCCAT Y Y CCGATTTGCTTTCTCTGACTTCC GGTGCCTCTAGTGCTGCCTG CAGGCAGCACTAGAGGCACC CATTTAGGGAGTGGCTACATTTTCC GGATACTAGCGTTGCGGTTGAG CGCTGAGATTY TCGGCCTTGGTAGGCAATGT U536Pr,L ietdGU256335 GU256305 GU256304 Peru, Cajamarca GU256319 GU256318 Peru, LaLibertad GU256355 GU256336 GU256355 GU256355 GU256335 CostaRica,Puntarenas CostaRica,SanJose prov. GU256355 CostaRica,Puntarenas GU256354 Mexico,Veracruz GU256353 GU256352 GU256340 GU256351 Mexico,Chiapas Mexico,Oaxaca GU256344 Guatemala,Quezaltenango GU256343 CostaRica, Alajuela GU256342 CostaRica(epiphyte) GU256341 GU256340 GU256339 Peru, Lima,Canta GU256289 GU256293 GU256292 Bolognesi Peru, Ancash, GU256290 GU256289 GenBank No. TCTGGGTCAACAACATCGCAC TTGAACTTTGCCACTCCTTTAGC GAAMAGGG Y TGGATACMCAAGAGTGG primersusedforPCRandsequencingof Sqec (5 Sequence Peru, Cajamarca Peru, Amazonas Peru, LaLibertad Peru, Amazonas Nicaragua, Granada Costa Rica Peru, Lima,Huarochiri Peru, Ancash,Aija Jaltomata Collection locality ¢ → 3 ¢ ) .

uan etal. 2006 uan etal. 2006 uan etal. 2006 uan etal. 2006 uan etal. 2006 GU256305 GU256319 GU256355 GU256293 source Identical to waxy waxy .

Copyright (c) American Society for Plant Taxonomists. All rights reserved. Delivered by Ingenta to IP: 192.168.39.211 on: Fri, 01 Oct 2021 12:59:15 habit =herbaceous. scored asfollows:corolla form=rotate, geography=South American, and ability, outgroups were removed from figures. For dered statesassumption as implementedinMesquite.To increase read- on theBayesianconsensustree usingaparsimonymodelwiththeunor- woody, suffruticose, andherbaceous. Ancestral stateswere reconstructed America, andtheGreater Antilles. Three stateswere recognized forhabit: regions were assigned:South America, widespread, MexicoandCentral and orange(traitvarieswithinthespecies),clear. Fourgeographic crateriform, androtate. Nectarcolorhasthree states: red toorange,clear were recognized: broadly campanulate,urceolate-tubular, shorttubular, to fruit color:orange,green, purple/black,andred. Fivecorolla forms scored ascategoricaldatawithmultiplestates.Fourstateswere assigned Maddison 2009 ). Fivemorphologicaltraitsandspeciesdistributionwere 2002). ( Swofford number anduncorrected pairwisedistancewere calculated usingPAUP* compared to procumbens cum Jaltomatadentata and sequences. out of142,115 totalpositions(0.20%) for58 dataset, 287DNA positionswere scored asmissingdata in theBayesiananalysesasbinary characters.Inthealigned of 2,598bases.Thirteen only afewbaseswere introduced tocreate atotalalignment lengths rangedfrom 2,405–2,457bases;numerous gapsof plus aportionofintron 10.Individual S.melongena and fiveoutgroup species.Three physaloidtaxaandthe beginning ofexon13were alignedforall waxy recover theposteriorprobabilities foreachclade. lengths wasmadeinMrBayesfrom theposteriordistributionoftrees to rule consensustree showingallcompatiblepartitionsandaveragebranch each run were grouped astheposteriordistributionoftrees. A majority- 155 all generationswere discarded asburn-in.Theremaining samplesfrom checked using AWTY ( Nylander etal.2008 ). Foreachrun thefirst25%of tion ofsplitfrequencies betweenruns stayedbelow0.01andgraphically of 0.10.Convergence wasdeterminedwhentheaveragestandard devia- allow swapratesbetweenchainstoexceedtheminimumsuggestedrate priate temperature valuewasdeterminedduringpreliminary runs to chains were incrementally heatedwithatemperature of0.15.Theappro- coupled Markovchainssampledevery100generations.Three ofthe Dirichlet distributionforthestatefrequencies), withfourMetropolis- distribution forthetransitionandtransversionrates,aflat(1,1,1) (0.0, 200)distributionforthegammashapeparameter, aBeta(1.0,1.0) modeled underanexponentialdistributionwithparameter10,auniform tree usingdefaultpriors(alltopologiesequallyprobable, branchlengths three parallelruns, eachof7,500,000generationsfrom arandomstarting ted toestimateparametersspecificeachmodel. Analyses consistedof MrBayes, codingsettovariable,andmodel-specificparameterspermit- MILLERET AL.: JALTOMATA PHYLOGENY included asasecondpartitionusingthebinarymodelimplementedin MrBayes version3.1.2( Ronquist andHuelsenbeck2003 ). Gapdatawere 2002). ( Swofford were calculatedbycomputingamajorityrule consensustree inPAUP* without improvement inthetopologyscore andbootstrapproportions Each pseudoreplicate wasautomaticallystoppedafter10,000generations replicates persearch andallstartingtrees created bystepwise-addition. tions were performedwiththesameparametersasabove,buttwo in thetopologyscore. Onethousandbootstrap( Felsenstein 1985 ) repeti- automatically terminatedafter20,000generationswithoutimprovement trees. Free modelparameterswere estimatedforeachsearch replicate and 20 searches were startedfrom stepwise-additiontrees and20from random 2011] Solanumlycopersicum Ancestral stateswere reconstructed inMesquite2.7.1( Maddison and Te The Published cpDNA geneswere compared todivergence levelswithin Bayesian phylogeneticanalyseswere performedusingtheprogram (EF438904)( Hu andSaedler2007 ) were compared for trnT-trnF for waxy Jaltomata (GU256344),and (DQ180418, DQ180419,DQ180450)( Weese andBohs2007 ); sequences from theendofexon 2through the Solanum lycopersicum sequenceswere availableonlyfrom exons2–10 (EF438985), and were compared for Solanum J. hunzikeri Jaltomata J. sinuosa

Results . . Jaltomata sinuosa (AP009280)for (GU256305)from thisstudywere (EF438939),and -specific gaps were included ndhF (AF500835,U47429, U08921) Jaltomata , , Solanum Jaltomata J. procumbens waxy Solanum lycopersi- Jaltomata matK . Substitution . , stateswere sequence . . species Jaltomata gene , and , for whichmaterial wasunavailable, species ofthegenus( Fig. 1 ). These twospecies(andanother unique combination oftraits:white,rotate corollas ( Fig. 4b ), and Clade 3bisawell-supportedgroup of port valuesbutlowML bootstrapvalues,exceptforclade3b. trees ineithersearch thatcontradicttheexistenceofclade3. ( Fig. 1 ). Thus,despitetheweaksupport,there are nooptimal ship betweenclade3a,2,andtheotherspeciesof3 the othersevenbest-scoringtrees failtoresolve therelation- clade 3aasthesistertorest ofthespeciesinclade3while tree are low, sixofthethirteenbest-scoringML trees support tree ( Fig. 2 ). Although supportvaluesforthisregion ofthe part ofaweaklysupportedclade3intheBayesianconsensus to theotherlineagesofclade3and2in Fig. 1 , butis J resolution ofthelineagecomprising low support(38BS/0.25PP). Bayesian tree ( Fig. 2 ) andsomeoftheML trees ( Fig. 1 PP). Clade3ismorphologicallydiverseandobtainedinthe ) with from MexicoandCentral America formclade2(93BS/1.00 purple-fruited other cladesare resolved from bothanalyses. All oftheblack/ ter totherest of (BS)/1.00 posteriorprobability (PP)from MrBayes) thatissis- lana in Fig. 1 . in Fig. 2 are when branchesresolved intheBayesianconsensustree tree 1. Fig. in Fig. 2 iscompatiblewiththestrictconsensusML tree in similar andthefullyresolved consensustree from MrBayes MrBayes. Theoveralltopologybetweenthetwoanalysesis tains aconsensustree showinginferred branchlengths from scoring trees from ML searches (-7,554.4935). Figure 2 branches. con- Figure 1 depictsastrictconsensustree ofthe13best results intopologybutdiffered insupportvaluesatsome sented bytwospecies, 4. Table in listed steps foreachparsimony-basedcharacterreconstruction is reconstructions are depictedin Figs. 4 and 5 . Thenumberof (0.0051). ter (0.012)asthemostdivergent chloroplast region, contains more thantwiceasmanysubstitutionspercharac- for Jaltomata 3d -42BS/1.00PP). has highBayesiansupport,butlowML BS(3c-24BS/0.91PP, and 3dinclude1719taxa,respectively, andeachgroup diversity incorolla formand nectarcolor( Fig. 4b ). Clades3c and encompass themajorityof well supportedclade(78BS/1.00PP).Thesetwosisterclades . “SanMiguel”(clade3a),whichisunresolved withrespect The other subcladesofclade3receive highBayesiansup- The maindifference betweenthetrees of Figs. 1 and 2 isthe The earliest-diverging clade(clade1)of Bayesian inference andML analysesproduced similar ld 1— Clade Reconstruction— State Ancestral Gene divergence within waxy and J. salpoensis J. auriculata Support valuesare includedforthebackboneof andpublishedcpDNA genes.Within and J. auriculata The earliestdiverging not present inthestrictconsensusofML trees Solanum Jaltomata Jaltomata (100BS/1.00PP).Clades3cand3dforma (Andes),whichare sistertotheremaining formsagroup (98%ML bootstrapvalue (oaee i smaie i al 3 Table in summarized is (Solaneae) (herbaceous, rotate corollas; Fig. 3a ) with72BSand0.40PP support.Two Jaltomata antillana Discussion Jaltomata Jaltomata Jaltomata neta caatr state character Ancestral andbetweenspeciesof speciesandmostofthe Jaltomata oppositifolia J. sanctae J . “purplering”( Fig. 3d ) (rae Antilles) (Greater lineage isrepre- - Jaltomata antil- martae Jaltomata trnT-trnF ) share a , , waxy and

Copyright (c) American Society for Plant Taxonomists. All rights reserved. Delivered by Ingenta to IP: 192.168.39.211 on: Fri, 01 Oct 2021 12:59:15 individual clades. Clade3isnotsupportedbyalloptimal ML trees, butisconsistentwithallML trees and issupportedbyth pseudoreplicates are includedabove branchesandposteriorprobabilities from Bayesian inference are belowbranchestoshowsup [Volume 36 SYSTEMATIC BOTANY 156 Fig. 1 1. Strict consensusof13best-scoringtrees from GARLI maximumlikelihood(ML)analyses.Maximumbootstrap pe Bysa analysis. Bayesian e port values rcentages of1,000 ³ 70%for Copyright (c) American Society for Plant Taxonomists. All rights reserved. Delivered by Ingenta to IP: 192.168.39.211 on: Fri, 01 Oct 2021 12:59:15 h branch. the for anoutgroup species, diverging branchesare includedwithML bootstrappercentages firstandposteriorprobabilities from Bayesian inference listed 157 MILLERET AL.: JALTOMATA PHYLOGENY 2011] Fig. 2. Majority-rule consensustree from MrBayesshowingallcompatible partitionsandaveragebranchlengths.Supportvalues Solanum lycopersicum , wasreduced, theactual length(1.33expectedchanges/site) isreported nexttothedouble hashmarkon second. Thebranch length forearly- Copyright (c) American Society for Plant Taxonomists. All rights reserved. Delivered by Ingenta to IP: 192.168.39.211 on: Fri, 01 Oct 2021 12:59:15 folia 5 SSEAI OAY [Volume 36 SYSTEMATIC BOTANY 158 side) (parsimony step #:18,9).Reconstructed nodesshowingequivocal statesare shaded gray. indicated, photos by T. Mione. Ancestral characterreconstructions: a) fruit color (parsimony step#:6);b)corolla form(left tubular corollas; h) Fig. ; d) . Crla iest aog among diversity Corolla 3. J . “purplering”;e-f)broadly campanulatecorollas; e) J. umbellata withalarge volumeofred nectar;i) Jaltomata species:a)rotate corolla of J. tayabambae J. bicolor J. grandiflora ; f) (726);j) J. “hummingbird”; g)shorttubularcorolla of ; b-d)crateriform-infundibularcorollas; b) J. bicolor (617),photobySegundoLeiva;k) side)andnectarcolor (right J. cajamarca J. yungayensis J. yacheri ; h-k)urceolate- . Exceptwhere ; ) c) ; J. oppositi- Copyright (c) American Society for Plant Taxonomists. All rights reserved. Delivered by Ingenta to IP: 192.168.39.211 on: Fri, 01 Oct 2021 12:59:15 (EF438904) ( Hu andSaedler, 2007 ) were compared for dentata trnF trnT waxy ndhF J.sinuosa Solanumlycopersicum and cies, Mexico andCentral America exceptfortwowidespread spe- J.grandiflora except fortwosuffructicose species, las ( Figs. 3a , black/purple fruits ( Fig. 4a 4b ) and bearpale-green, rotate corol- ). Theseare primarilyherbaceousplants, ( Mione etal.1994 ). cies producing orangefruits (clade 3)withstrong support grouped previously withotherSouth American cpDNA restriction siteanalysis,thesetwospecies havebeen in thetwophylogeneticanalyses(72bs/0.40PP).Basedon phyly oftheremaining species showmoderatetolowsupport this lineageassistertotherest of is herbaceousexceptforawoodybase( Fig. 5b ). Supportfor red fruits ( Fig. 4a ), andasuffruticose habitwhere theplant 159 MILLERET AL.: JALTOMATA PHYLOGENY 2011] ance throughout itsrange.Bothspecieswere sampledonly able species,whereas 5a). ( Fig. North America, Central America, andwestern South America matK Reconstructed nodesshowingequivocalstatesare shadedgray. gene Table 2— Clade Fig. (DQ180418, DQ180419,DQ180450)( Weese andBohs2007 ); - Solanum lycopersicum

trnF cl9222–600250.0258–0.279 0.00215 24–26 2 932 chl Jaltomata procumbens 4 4. Ancestral characterreconstructions: a)geography, lomasspeciesindicatedwithan‘L’ (parsimonystep#:4);b)habit (EF438985), (GU256305)from thisstudywere compared. cl19210 1,972 chl . ee oprsn bten between comparisons Gene 3. genome Jaltomata procumbens nuc chl The ninespeciesinclade2generallyproduce ( Fig. 5b ). Speciesare narrowly distributedin sequence aligned J. hunzikeri 2,598 2,086 (AP009280), length for J. repandidentata ndhF Jaltomata and 29 # sitesdifferent (EF438939),and 4 (AF500835, U47429,U08921)and Jaltomata procumbens

J. repandidentata isamorphologicallyvari- 175–180 Solaneae Jaltomata 39–43 75 0.005 47–53 Jaltomata sinuosa isuniforminappear- Jaltomata bohsiana 0.01185 0.00192 Jaltomata isweak;themono- uncorrected “p”distance Solanum lycopersicum (GU256344),and

matK , of southern Jaltomata , , J. procumbens 0.0765–0.0788 0.0187–0.0206 0.0269–0.0304 . For Solaneae Jaltomata and spe- waxy trnT- , ,

egah 5a 4b 4b 4 9 18 geography nectar color corolla form habit fruit color change from anyonestatetoanother. Mesquite’s unordered parsimonymodel. A parsimonysteprepresents a 3 b) To pce, species, Two 4b). 3e–k, clades of Species 3c and3dvaryincorolla shapeandnectarcolor( 3c–d,4b). (Figs. Figs. 3b corollas infundibular , to form Species ofbothclades3aand3bbearflowerswithcrateri- logeny, butthebranchingorder haslowsupport( Figs. 1 – 2 color ( ). Fig. 4b ). Foursubcladesare resolved inthe diverse incorolla colorand corolla form( Fig. 4b ) andinnectar South America ( Fig. 5a ), these speciesare morphologically by theseshared traits.Predominately distributedinwestern port inthephylogeneticanalysis,butisfurthersupported ( Fig. 4a ), shrubby ( Fig. 5b ). Clade3hasonlyweaksup- 2). ( Table dentata many speciesgroups elsewhere in imens sampled,andwithsequencedivergence comparableto variable also,withfiveuniquesequencesamongthesixspec- America) forthisstudy. in thenorthernportionoftheirrange(MexicoandCentral tinct floralbowlwhere nectarpools,asopposedtopooling both species,thefusionofstaminalbasescreates adis- a distinctstamen,style,andstigmamorphology( Fig. 3f ). In bird,” are sistertotheremaining speciesofclade3candshare Character Table Cae 3— Clade isgeneticallyuniformforthefivecollectionssampled 4. Ancestral characterstatereconstruction performedusing Species ofclade3are generallyorange-fruited Jaltomata aspera Jaltomata procumbens Parsimony Steps 7 6 Jaltomata and (parsimonystep#:7). , while isgenetically J. “humming- waxy J. repandi- phy- Figure 5b 4a Copyright (c) American Society for Plant Taxonomists. All rights reserved. Delivered by Ingenta to IP: 192.168.39.211 on: Fri, 01 Oct 2021 12:59:15 species. Theorange-fruited lineagesofclade3are woody Clade 2isgenerally herbaceouswithonly two suffruticose herbaceous exceptforaportion ofstemclosetotheground. species inclade1are bothsuffruticose; plantsare generally had identicalsequences( Table 2 ). accessions from theDepartmentof Ancash were sampledand (617) haveapurple,tubular-urceolate corolla ( Fig. 3j ). Two tubular corolla ( Fig. 3i ), whereas collectionsfrom Lima,Peru from Ancash, Peru (726)haveagreen, nearlystraight- a monophyleticgroup withinclade3d( Fig. 1 ). Collections bear corollas thatdiffer inshapeandcolordonotform The twoformscollectedindifferent departmentsofPeru assessment ( Fig. 1 ). but alackofresolution betweentheselineagescloudsthis in nectarof ored nectarremains unstudied.Redpigmenthasbeenstudied however, thepollinationbiologyof observed visiting [Volumelate ortubularcorollas ( 36 Fig. 4b ). Hummingbirds havebeen corollas andred nectarpersistedindescendantswithurceo- urceolate-tubular corollas haveevolvedfrom campanulate morphology haschanged,exceptinsomeinstanceswhere is true, thenred nectarcolorhas been lostwhencorolla junction withtheevolutionofcampanulatecorollas. Ifthis have evolvedseveraltimesindependently, possiblyincon- nator preference. Red/orangenectarcolorationappearsto nectar mayimplicateconvergence forthesetraitsbypolli- do aswell. A correlation betweencorolla shapeandcolored and asubsetofthespecieswithtubular-urceolate corollas broadly campanulatecorollas produce red/orange nectar a monophyleticgroup ( Fig. 4b ). All SYSTEMATICsynapomorphy. BOTANY the fusionofstaminalbasesin ( Fig. 4b ). Thedatasupportthedistinctfloralbowlcreated from rotate withinclade3din from crateriformcorollas includingtworeversals backto ( Fig. 4b ). Thevariousothercorolla shapesmayhaveevolved eral speciesandisinferred tobetheancestralformforclade3 ( Fig. 4b ). Thecrateriformcorolla ( Figs. 3b Bohs etal.2007 -d) occursinsev- ), suggestingitastheancestralformin in allbutafew las are foundintheearliest-diverging lineagein form appearingtohaveevolvedmultipletimes.Rotatecorol- is broadest atthebaseandnarrows distally. capitate asinotherspecies;thesetwospecieshaveastylethat on thecorolla asinother 160 and may haveevolvedtwicewithinclade3c( Berries thatsplitopenwhenripetoreveal themature seeds rity seemstorepresent acaseofneotenyinfruit development. green whenimmature, theretention ofgreen colorintomatu- black-fruited lineages( Fig. 4a ). Sinceall least three timesindependently from withinbothorange-and and characterizeonemajorclade.Green berriesevolvedat to beancestralin from thepurple/blackfruits, thenred/orange fruits appear fruits represent quantitativevariationinfruit color, asdistinct and role inpollinationremains unclear( Olesen etal.1998 ). Each cladeexhibitsacharacteristichabit( Fig. 5b ). Thetwo Variants of Jaltomata Evolution— Character If clade1issistertoother J . . sanchez-vegae speciesproducing red-colored nectarare not Nesocodon Jaltomata bicolor Solanum Jaltomata J . “hummingbird” (T. Mione, pers.observ.); , T. M.andS.LeivaG.,fieldobservations), (Campanulaceae),yetitssignificance species( Nee 1999 ; Hunziker 2001 ; Corolla shapeislabile,witheach . Purple/blackberriesevolved once Jaltomata Jaltomata J. aspera mayrepresent distinctspecies. Jaltomata species.Thestigmaisnot “libertadii”and Jaltomata and Jaltomata andifred or orange J . “hummingbird” asa Jaltomata Jaltomata chotanae specieswithcol- specieswith Jaltomata fruits are J. sinuosa Jaltomata and

are indeedsuffruticose, theancestralhabitof ally exhibitasuffruticose habit.Ifmanyherbaceousspecies field butimpliesthatspecieslabeledasherbaceousmayactu- greenhouse-grown plants.Thisfeature wasnotvisibleinthe in theherbaceousspecies, field (T. Mione,pers.observ.), butanexposedwoodycaudex equivocal. Mostofthesespecieshabitswere confirmedinthe is suffruticose. Thus,inference regarding ancestralhabitis except forthree species,twoofwhichare herbaceous andone Greater Antilles. Greater Antilles. U. S. A., toBolivia,ontheGalapagosIslands,andin be inferred tobesuffruticose. DAc, . 99. Te lsiiain f h Slnca P. 3–4 n in 3–48 Pp. Solanaceae. the of classification The 1979 . in G. 73–133 W. D’Arcy, Pp. angiosperms. in pollination Buzz 1983. L. S. Buchmann, and Wagenen , van A. Thomas, N. Lefgren , V. Myers, N. Weese , T. L., Bohs, 1973. R. S. Altschul, (to TM)andNSFDEB-0542493toRGO. Support wasfrom research grantsfrom theNationalGeographicSociety one anonymousreviewer fortheirvaluablecommentsonthemanuscript. Bohs forspecimensincludingseeds.Finally, wethankDavidSpoonerand in NicaraguaandCostaRica,respectively, andDavidSpoonerLynn fieldwork inthe Andes, FelixCoeandBillHaberforhostingfieldwork Bernardello forhelpfuldiscussion, SegundoLeivaG.andLeon Yacher for distributed thananyother. cally uniform,theblack/purple-fruited cladeismore widely ( Fig. 5a ). Although lessspecies-richandmore morphologi- successfully colonizedMexicoandCentral America once ancestor mayhaveoriginatedinSouth America andthen once aftermultipledispersaleventsfrom the Andes. invoked, theabilitytoliveinlomashasevolvedmore than times bydifferent Andean lineages.Whichever scenariois nities. Instead,colonizationmayhaveoccurred anumberof lomas speciesdiversifiedandcolonizedothercommu- the lomasrepresentatives, itseemsunlikelythatanancestral on virtualislands.Giventhephylogeneticdistanceamong closely related, butgrow some190kmawayfrom eachother (J.procumbens of widespread speciesthat dispersedbacktoSouth America predominantly inMexico andCentral America withacouple J.auriculata phologically andgeneticallysimilartotheSouth American America (exceptfor the remainder ofthe the black/purple-fruited, primarilyMesoamericanclade, and weinferthat likely originatedinSouth America ( Olmstead etal.2008 ) not from thelomas). plant from whichDNA wasextracted from the Andes, in thelomasand Andes (therepresentative species oftheearlydiverging lineageofclade3c,grows both lana phyletic. Three speciesof clade3d, Biogeography— Acknowledgments. Te The The black/purple-fruited cladeof and n A D Sedn odn: Aaei Press . Academic London: Skelding. D. A. and biology andtaxonomy oftheSolanaceae Inc. Co., Reinhold Nostrand Van York : New Little. Handbookofexperimentalpollination biology in heteranthery genetic context and . Zygomorphy 2007. Stern. S. Press. University Harvard Jaltomata J. umbellata ). and speciesofthePeruvian lomasare notmono- Solanum Acta Horticulturae Drugs andfoodsfrom little-known plants Jaltomata Jaltomata J. repandidentata). are confinedtolomas,while We thankGregory J. Anderson andGabriel Jaltomata J. antillana ieaue Cited Literature Jaltomata truxillana , thesistergroup of J. speciesoccurfrom Arizona, “hummingbird” wasobservedin didaswell( Fig. 5a ). Exceptfor cladesare restricted toSouth 4: 201–223. 745: inclade1,whichismor- , d. J G Hwe , . . Lester , N. R. Hawkes, G. J. eds. , Jaltomata lomana,J A black/purple-fruited A Jaltomata , d. C E Jns n R J. R. and Jones E. C. eds. , and Solanum Jaltomata Jaltomata isdistributed J. lomana . Cambridge: . J inaphylo- . . aspera J . . . . would , most , truxil- aspera are The , a ,

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La Libertad, & L Yacher 730 J.sagastegui Hunz., CostaRica,Puntarenas, T. Mione&L.Yacher 691 GU256353; (Dunal) Hunz.,CostaRica,Puntarenas, Hunz., Mexico,Veracruz, T. Mione&F. Coe555 J.procumbens 460 & Kunth)M.NeeMione,Ecuador, Carchi, S. Leiva&Mione,Peru, LaLibertad, (CONN), GU256329; GU256295; GU256313. J.yungayensis corolla”, Mexico,Mexico D.F., S. Leiva,Peru, Cajamarca, Cajamarca, T. Mioneetal.725 Peru, LaLibertad, J.salpoensis (CCSU), GU256311; (CCSU), GU256334; 697 GU256341; (Cav.) J.L.Gentry, CostaRica, Alajuela, Costa Rica, D.Spooneretal.959a 7035 bens S. Leiva,Peru, Cajamarca, Mione, Peru, Cajamarca, La Libertad, Mioneetal.637 631 T. Mioneetal.733 J.sanchez-vegae S. Leiva&Mione,Peru, LaLibertad, Peru, LaLibertad, T. Mioneetal.706 (CCSU), GU256336; (CCSU), GU256294; Mione, Bolivia,LaPaz, or 6508 J.lezamae J.leivae S. Leiva&Mione,Peru, Cajamarca, et al.708 (CCSU), GU256338; (CCSU), GU256319; bird”, Peru, LaLibertad, Libertad, 349 1114 and Greenmann) D’Arcy, Mione&Davis,Mexico,Michoacan, (HAO),GU256312; (CCSU),GU256340; (NY),GU256297; (CONN),GU256345; (Cav.) J.L.Gentry, Mexico,Chiapas, (MO),GU256350; (BIGU),GU256342; (F),GU256306; Mione,Peru, Cajamarca, (CCSU),GU256304; S.Leiva&Mione,Peru, Cajamarca, T. Mioneetal.713 Mione,Peru, Cajamarca, J. procumbens J. umbellata S.LeivaG.&Mione,Peru, LaLibertad, J. repandidentata T. Mioneetal.670 T. Mione&L.Yacher 692 (Cav.) J.L.Gentry, Guatemala,Quezaltenango, T. Mioneetal.718 Mione&S.Leiva,Peru, Ancash, T. Mioneetal.712 S.Leiva&Mione,Peru, Cajamarca, (CCSU),GU256296; (CCSU),GU256291; (CCSU),GU256335; (CCSU),GU256324; (HAO),GU256305; T. Mioneetal.647 T. Mioneetal.722 J. repandidentata J. lojae (CCSU),GU256343; J. J. sinuosa J. salpoensis J. J. lomana J. mionei “SanMiguel,”Peru, Cajamarca, (RuizLópez&Pavón)Mione,Peru, Lima, “rednectar”, Peru, Cajamarca, J. (Cav.) J.L.Gentry, CostaRica, J. J. (CONN),GU256351; “libertadii”,Peru, LaLibertad, Mione etal.564 J. procumbens Mione etal.674 J. weberbaueri “green fruit,” Mexico,MexicoD.F., “purplering”,Peru, Cajamarca, Mione &Leiva758 J. guillermo-guerrae Mione 571 T. Mioneetal.737 (CCSU),GU256354; Mione,Ecuador, Loja, Mione etal.705 (CCSU),GU256314; (Dunal)Hunz., Costa Rica,SanJoseprov., Mione&S.Leiva,Peru, Ancash, (Miers)Mione,Peru, Amazonas, LeivaG.&Quipuscoa,Peru, LaLibertad, J. sinuosa T. Mione&W. Haber696 T. Mione&R.Bye602 (CCSU),GU256320; (F),GU256325; , GU256317; S.LeivaG.&Mione,Peru, Amazonas, T. Mioneetal.660 T. Mioneetal.741 (CONN), GU256352; (Dunal)Hunz.,Nicaragua,Granada, T. Mioneetal.755 T. Mioneetal.715 J. nigricolor (CCSU),GU256318; (Cav.) J.L.Gentry, Mexico,Oaxaca, (CCSU), GU256339; T. Mione&S.LeivaG.759 (Dammer)Mione,Peru, Ancash, J. ventricosa J. sanchez-vegae (CCSU),GU256316; J. yacheri (Miers)Mione,Peru, Cajamarca, (F),GU256337; (LPB),GU256321; J. tayabambae T. Mione&L.Yacher 699 J. procumbens T. Mione&L.Coe605 (CCSU),GU256326; Mione 401 (CCSU),GU256323; (CCSU),GU256333; Mione&S.Leiva,Peru, La J. viridiflora M. O.Dillonetal.6505and/ T. Mioneetal.723 S.Leiva&Mione,Peru, J. repandidentata Mione&S.Leiva,Peru, J. oppositifolia J. repandidentata J. herrerae T. Mione&S.McQueen D. M.Spooneretal.5037 (Baker)Mione,Peru, (CONN),GU256331; (CCSU),GU256310; (CCSU),GU256344; (CCSU),GU256346; (CCSU),GU256328; S.Leiva&Mione, (CCSU),GU256322; (CCSU),GU256355; J. yacheri T. Mione&W. Haber S.Leiva&Mione, (Cav.) J.L.Gentry, T. Mioneetal.742 T. Mioneetal.740 T. Mioneetal.639 T. Mioneetal.738 J. paneroi T. Mioneetal.650 (Humb.,Bonpl. J. repandidentata (C.V. Morton) Leiva etal.3647 J. sanchez-vegae D. Spooneretal. J. J. procumbens “humming- S.Leiva& J. truxillana Mione etal. Mione& J. procum- J. Mione& (CCSU), (Dunal) (CCSU), (CCSU), (CCSU), (Dunal) T. Mione T. Mione “yellow “yellow T. Mione J. lanata Davis