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Systematic Botany 29 SystematicBotany (2004),29(1): pp. 147– 164 q Copyright 2004by the AmericanSociety of PlantTaxonomists Paraphyly in Tribe Onagreae: Insights into Phylogenetic Relationships of Onagraceae Basedon Nuclear and Chloroplast Sequence Data RACHEL A. LEVIN,1,7 WARREN L. WAGNER,1 PETER C. HOCH,2 WILLIAM J. HAHN,3 AARON RODRIGUEZ,4 DAVID A. BAUM,5 LILIANA KATINAS,6 ELIZABETH A. ZIMMER,1 and KENNETH J. SYTSMA5 1DepartmentofSystematic Biology,Botany,MRC 166,Smithsonian Institution,P.O.Box 37012,W ashington, District ofColumbia 20013-7012; 2Missouri BotanicalGarden, P.O.Box 299,St. Louis, Missouri 63166-0299; 3108White-Grav enor,Box 571003,Georgetow nUniversity,Washington,District ofColumbia, 20057-1003; 4Departamento de Botan ´‡ca y Zoolog´‡a,Apartado Postal 139, 45101 Zapopan, Jalisco, M exico; 5Department ofBotan y,University ofW isconsin, 430Lincoln Drive,Madison, Wisconsin 53706; 6DepartamentoCienti co de PlantasV asculares,M useo de Ciencias Naturales,Paseo del Bosques/ n, 1900La Plata, Provincia de Buenos Aires, Argentina 7Author forcorrespond ence ([email protected]) CommunicatingEditor: Thomas G .Lammers ABSTRACT. Onagraceaeare afamilyof 17 genera insev en tribes,with the majorityof species intribes Onagreae and Epilobieae.Despite the species-richnessof these twotribes,to date no phylogenetic studyhas been done withsuf cient taxon samplingto examine relationshipsbetw een and withinthese tribes.In this study ,we used DNAsequence data from one nuclear region(ITS) and twochloroplastregions ( trnL-trnF and rps16)to inferphylogene tic relationshipsamong93 taxa across the family,withconcentra ted sampling inthe large tribeOnagreae .Results stronglysuggest tha ttribeGongylocarpeae issister to tribes Epilobiea e 1 Onagreae,bothof which are monophyletic. WithinOnagreae , Camissonia seemsto be broadly paraphyletic, and Oenothera isalso paraphyletic. In Oenothera thereappear to be twolineages, one ofwhich has Gaura 1 Stenosiphon nested withinit. Atthe base ofthe Onagraceaephylogeny,wehave claried previousconfusion regarding conicting placemen tsof Hauya and Lopezia based on nuclear versuschloropla stda ta. Results ofthese analyses are supported bymorpholo gyand suggestthe need fornew taxonomicdelimitations, which are forthcoming. The plantfamily Onagraceae(Evening-p rimroses) Clarkia (Sytsmaan dSmith 1988,1992; Sytsma et al. comprises ca.655 species across17 genera (Levin et al. 1990;Gottlieb and Ford 1996;F ord and Gottlieb2003; 2003),with atleast twothirds ofthe species occurring W.J.Hahn et al.,in mss.), Epilobium and Chamerion in tribes Onagreae (8genera, 262spp .)and Epilobieae (Baumet al.1994), and Gaura (Hoggard et al.,2004). (2genera, 172spp .).Onagraceae have aworld-wide However, no such study has focusedon relationships distribution, with the majority ofspecies concentrated among tribes Onagreae and Epilobieae.Furthermore, in the New World, especially western North America. within Onagreae there have been no molecularphy - Over the pastfew decades, the family has developed logenetic studies ofthe species-richgenera Camissonia asa model system forstudying plante volution.Com- (62spp .;w estern North America,1 sp.in SouthAm er- parativestudies ofcytology ,embryology,palynology, ica) and Oenothera (120spp .;Americas, the majority of anatomy,morphology,reproductive biology,and species in western North America). chemistry have allbeen completed forv ariousgroups Using chloroplast rbcL and ndhF sequence data,Le v- within the family (reviewedin Raven 1988).U nfortu- in et al.(2003) showed thatthe small genus Gongylo- nately,alimitation ofthese previous studies has been carpus (2spp .),previous ly included in tribe Onagreae the absenceof a robustph ylogeneticframeworkwithin (Raven 1964,1979; M unz1965), is strongly supported which toexamine the evolution ofthese traits. assister tothe rest ofOnagreae 1 Epilobieae,and Todate there have been several molecular (Martin should beplaced in its own tribe,Gongylocarpeae. and Dowd 1986;Crisci et al.1990; Sytsma et al.1991b; That analysis alsosuggested thatneither Camissonia Bult and Zimmer 1993;Conti et al.1993) an dmorpho- nor Oenothera is monophyletic,although sampling logical (Hochet al.1993) ph ylogeneticstudies ofthe within these genera waslimited. Camissonia appears family,although only recently has there been amolec- tolack an ymorphological synapomorphies (Raven ularstudy thatincluded members ofall Onagraceae 1969;H ochet al.1993), and the only characteruniting genera (Levin et al.2003). There have alsobeen various Oenothera (stigma with 4linear elongate non-commis- phylogenetic studies ofindividual genera within the sural lobes)also characterizes Stenosiphon and Gaura family,including Fuchsia (Sytsmaand Smith 1988, (Hochet al.1993; H oggard et al.,2004); howe ver, Sten- 1992;Sytsma et al.1991a; P .Berry et al.,U .Wisconsin- osiphon and Gaura differ because ofthe presence ofan Madison, in mss.), Lopezia (O’Kane and Schaal1998), indusium atthe baseof the stigma lobes. 147 148 SYSTEMATIC BOTANY [Volume 29 Thus, amajor goalof the present study is toun- inour study,and instead we included bothsubspecies of G. hex- andra (sect. Pterogaura).In the othersix tribes, tw otaxa were sam- derstand relationships between and within tribes On- pled from Ludwigia (tribeJussiaeea e)to serveas amonophyletic agreae and Epilobieae,with aparticularemphasis on outgroup forphylogen etic analyses, given previousstudies that evaluating the monophyly ofthe large and diverse unambiguouslyplace thisgenus sisterto the restof Onagraceae genera Camissonia and Oenothera.Aphylogenetic (e.g., Levin et al. 2003). Onespecies each fromtribes Ha uyeae, Fuchsieae,Circaeeae,and Gongylocarpeae was also included. In frameworkwill facilitatecomparativ eanalyses ofchro- orderto moreprecisely determinethe relationship ofthe newly mosomal evolution and pollination biology ofthese di- described monotypicgenus Megacorax to Lopezia (tribeLopezieae ), verse groups, aswell asbiogeograph icalstudies ofthe wesampled four Lopezia species fromv arious sectionsplus Me- gacorax gracielanus . The cp trnL-trnF and nuclear ITSregions w ere radiation ofthese tribes in southwestern North Amer- sequenced froma total of93 taxa. The cp rps16 regionw as se- ica(Katinas et al.2004). quenced froma subsetof 75 species focused mainlyin Onagreae , While the main focusof this study is on Onagreae inorder to improve resolutionwithin this species-rich tribe.All and Epilobieae,wehaveincluded sampling from mem- taxa included inthis study are listedin T able 1withvouche rin- formation. bers ofall Onagraceae genera. This strategy is not only DNAExtraction, Amplication, and Sequenc ing. Total genomic important forexamining relationships among tribes DNAforthe majorityof taxa was provided byKJS (see protocols Onagreae and Epilobieae,butinclusion ofDN Ase- inConti et al. 1996; Sytsmaet al. 2002). However, several taxa were quence datafrom bothn uclearand chloroplast regions extracted bythe seniora uthorfrom either silica gel-driedor her- barium material usingthe QiagenDneasy y kit(Qiagen Inc., Va- allows examinationofprevious conict among evolu- lencia, CA).DN Asof Lopezia lopezioides , L. racemosa, and L. lang- tionary reconstructions based on these twogenomes maniae were provided byS. O’ Kane (Univ.NorthernIo wa), and and on morphology,especially aspertains tothe place- DNAs of Oenothera deltoides and O. pallida were provided byM. Evans (Univ.Arizona). ment of Hauya and Lopezia (Bultand Zimmer 1993; ITS.Ampli ca tionof the internal transcribedspacer (ITS)re- Conti et al.1993; H ochet al.1993; Levin et al.2003). gionof nuclear ribosomalDN A, composed ofITS1, the 5.8S gene, The recently described genus Megacorax (Gonza´lez Eli- and ITS2(Baldwin 1992; Baldwin et al. 1995) was mainlycon- zondoet al.2002) may bevital todiscerning relation- ducted byWJH using primers ITS4 (5 9-TCCTCC GCT TATTGA TAT GC-39;Whiteet al. 1990) and ITS5HP (5 9-GGA AGG AGA ships of Hauya and Lopezia tothe rest ofthe family,as AGT CGT AACAAGG-3 9;Hershkovitz and Zimmer1996); these Levin et al.(2003) found that Megacorax is sister to Lo- primersw ere also used forthose ampli ca tionsdone bythe senior pezia.Because sampling of Lopezia species waslimited author.Standard PCR conditions were used, although Ready-to- goPCR beads (AmershamPharmacia Biotech Inc.)w ere employed in thatstudy ,it wasunclear whether Megacorax should fora fewtaxa that were difcult toamplify. PCR products were beplaced within Lopezia.Thus, the present study in- cleaned usingP EG precipitation and ethanol cleaning (Morgan cludes additional sampling from varioussections of and Soltis1993). Cycle sequencingused ABIBig Dye chemistry Lopezia (Plitmann et al.1973; O’ Kane and Schaal1998). (Applied Biosystems,Foster City ,CA),and was done inboth di- rectionsusing the same primersas forampli cation. Additional In this paperw eendeavor to:1) examine relation- sequencingprimersw ere used byWJH, including ITS2(5 9-CGT ships between and within tribes Onagreae and Epilo- AGC TACTTC TTG CATCG-3 9;Whiteet al. 1990), ITS3B(5 9-GCA bieae,2)test the monophyly of Camissonia, Oenothera, TCG ATG AAGAACGTAGC-3 9;Whiteet al. 1990), and C5.8S 9 9 and Gaura,3)compare signal from nuclearvs. chlo- (5 -TGC GTT CAAA GACTC GAT-3 ;Suhet al. 1993). ITSse- quences for Lopezia lopezioides , L. racemosa, and L. langmaniae were roplastdata, especially asit relates toearlier conict provided byS. O’Kane (Univ.NorthernIow a), and the sequences regarding relationships of Hauya and Lopezia, and 4) for Chamerionangustifolium , all Epilobium species, and Clarkia
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