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An ITS-Based Phylogenetic Analysis of the Perennial, Endemic Apiaceae

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An ITS-Based Phylogenetic Analysis of the Perennial, Endemic Apiaceae SystematicBotany (2004),29(2): pp. 419– 431 q Copyright 2004by the AmericanSociety of PlantTaxonomists An ITS-BasedPhylogenetic Analysis ofthe Perennial, Endemic Apiaceae Subfamily Apioideae ofWestern North America FENG-JIE SUN,1 STEPHEN R. DOWNIE,1,3 and RONALD L. HARTMAN2 1Department ofPlant Biology ,University ofIllinois atUrbana-Cham paign, Urbana,Illinois 61801; 2DepartmentofBotany ,University ofWy oming, P.O.Box 3165,Laramie ,Wyoming 82071 3Author forCorrespon dence ([email protected]) CommunicatingEditor: John V .Freudenstein ABSTRACT. Phylogenetic analyses of159 DNAsequencesfromthe nuclear rDNAinternal transcribedspacer regionw ere conducted toev aluate the monophylyof the herbaceous, perennial genera ofApiaceae subfamilyApioidea eendemic to NorthAmerica (northof M exico) and todetermine the relationships ofthose elements that currentlycomprise Cymopterus withinthe group.The resultsof a previous phylogenetic studyw ere equivocalinsuggesting monophyl yforthese perennial, endemic taxa and revealed Cymopterus tobe polyphyletic, withits species closely linkedwith those of Aletes, Lomatium, Musineon, Oreoxis, Orogenia, Podistera, Pseudocymopterus , Pteryxia, and Tauschia.Herein, weexpand samplingto include com- prehensiverepresentationof Aletes, Cymopterus, Musineon, Oreoxis, Orogenia, Podistera, Pseudocymopterus , and Pteryxia, and greaterrepresenta tionof Lomatium and Tauschia.Wealso include all membersof tw ogenera notexamined previously, Glehnia and Oreonana,as well as additional outgroup genera fromthe Angelica clade ofthe apioid superclade. Ourresults indicate that the perennial, endemic apioid umbellifersof N orthAmerica constitute a(weakly supported) monophyletic group,with Angelica and the meso-American Arracacia clade comprisingtw oofseveral possible sistergroups. The twosubspecies of Glehnia littoralis ally with Angelica and Peucedanum japonicum ; Oreonana showsaf nity with several species of Cymopterus and Lomatium.The lack ofresolution in the ITStrees preclude sunambiguous hypothesesof relationsh ip amongthese perennial, endemic umbellifersbut does show that manyof these genera, where resolved, are notmonophy letic. Indeed, Cymopterus and Lomatium are highlypolyphyle tic and permeate all majorclades resolved inthe molecule-derived trees. Evidence from branch lengthsand low sequence divergencesuggeststhat thisgroup ofN orthAmerican umbellifersunderw ent rapid radiation, likelyduring the geoclimatic eventsof the Late Tertiaryand Quaternary. Cymopterus Raf.(Apiaceae subfamily Apioideae ), Oreonana Jeps., Oreoxis Raf., Orogenia S. Watson, Podis- the spring-parsleys, comprises some35species (Kar- tera S. Watson, Pseudocymopterus J.M.Coult. & Rose, tesz 1994)of herbaceous perennials distributed largely Pteryxia (Nutt.ex Torr.&A.Gray) J.M. Coult. & Rose, throughoutw estern North America (NA).Approxi- and Shoshonea Evert &Constance (Mathias1930; Evert mately two-thirds ofthese species are restricted tothe and Constance 1982;Downie et al.2002). All are pe- GreatBasin region, roughly bounded bythe SnakeRiv- rennial taprootedherbs and many are similar to Cy- er ofIdaho, Sierra Nevadaof California, Colorado Riv- mopterus in their primarily low-growing and acaules- er ofArizona, and the Rocky Mountains ofColorado cent or subcaulescenthabit. Lomatium is the largest ge- (Mathias1965). Many species are xerophytic or semi- nus,with 78species; Glehnia, Harbouria, Neoparrya, and xerophytic,being conned todry ,sandy,or alkaline Shoshonea are monospecic, and the remaindercom- habitats.They are low in stature,possess thickened, prise some 2–6 species each(Kartesz 1994). Consider ed deep taproots,and have ternately cleft,com pound or collectively,these plants present such aconfusing in- dissected leaves. The inorescence is an open com- tergradation ofsimilar characteristicsthat generic de- pound umbel,and the owers are mostly yellow or limitation is made exceedingly difcult, and in the ab- white,opening from very early in the spring to sence ofmature fruits, many species are essentially in- throughoutthe summer.Most distinctive,however, is distinguishable(J ones 1908;Mathias 1930; Theobald et their fruit,for the twomarginal (lateral),and usually al.1963; W eber 1984;Cronquist 1997;Downie et al. one or more ofthe three dorsal ribs, are conspicuously 2002).Cronquist (1997)included Oreoxis, Pseudocymop- winged. These wings may bem embranous tospongy- terus, and Pteryxia within abroadly circumscribed Cy- corky,and variously plane tow avy or corrugated.In- mopterus (Hitchcockand Cronquist 1961;Cronq uist deed, the generic nameis derived from the Greek 1997).Cronq uist (1997)also stated thatthe distinction kyma, a wave, and pteron, awing, referring tothe often between Cymopterus and Lomatium,i.e.,the conspicu- undulate wings ofthe fruit. ously winged dorsal fruitribs ofthe former,‘‘is subject Muchconfusion exists with regard tothe proper tofailure .’’Phylogeneticstudies ofthese endemicand delimitation of Cymopterus and its relationship tothe largely cordilleran genera are few and havefocused other indigenous umbellifers ofw estern NA(whose almost exclusively upon Lomatium (Schlessman 1984; ranges extend from southern Canadato northern Mex- Simmons 1985;Gilmartin and Simmons 1987;Soltis et ico).These genera include Aletes J.M.Coult. & Rose, al.1995; Soltis and Novak1997; Hardig and Soltis Glehnia F.Schmidt ex Miq., Harbouria J.M.Coult. & 1999). Rose, Lomatium Raf., Musineon Raf., Neoparrya Mathias, Results from aprevious phylogenetic study of85 419 420 SYSTEMATIC BOTANY [Volume 29 species ofN Aapioidumbellifers revealed that Cymop- from the Angelica clade ofthe apioidsuperclade terus (17examined species) and Lomatium (28 exam- (Downie et al.2001)— speci cally ,the perennial, cir- ined species) are eachpolyph yletic, with their species cumborealgenera Seseli L., Selinum L., and Peucedanum intertwined with those of Aletes, Musineon, Oreoxis, Or- L. Our major objectives are toev aluatethe monophyly ogenia, Podistera, Pseudocymopterus , Pteryxia, and Taus- ofthe perennial, endemic genera ofN A(north ofM ex- chia Schltdl. (Downie et al.2002). Closely allied were ico)and toascertain the phylogeneticrelationships of three genera ofcentral toeastern NAdistribution[ Po- those elements thatcurrently comprise Cymopterus lytaenia DC., Taenidia (Torr.&A. Gray)Drude ,and within this group.Wecontinueto utilize the nuclear Thaspium Nutt.] and Zizia W.D.J.K och,the latter dis- rDNAinternal transcribed spacer(ITS) region forph y- tributed widely acrossN A.Our observations ofmature logenetic inference,given the wealth ofITS seq uence fruitcross-section s, aswell ascladistic analysis ofmor- dataalready accumulated forth eApiaceaefor com- phological characters,con rm ed thatthose character- parativepurposes, their faster substitution rates com- istics ofthe fruitused traditionallytodiagnose genera pared toloci from the chloroplast genome (Downie et (suchas wing shape and composition,and the orien- al.2001), and their utility in resolving relationships tationof mericarp compression)are indeed highly var- among congenericspecies ofApiaceae (Soltis and Ku- iable,thus severelylimiting their usefulness in phylo- zoff1993; Downie and Katz-Downie1996;V argas et al. genetic estimation.The results ofDownie et al.(2002) 1999). veried the close relationship among these genera, but were surprising in suggesting ane volutionary history MATERIALSAND METHODS ofthe group muchmore complicatedthan previously considered. TaxonSampling. Complete ITS-1and ITS-2sequences for74 accessions ofApiaceae subfamilyApioidea eare reported here for The restricted distributionofmany endemic,w est- the rsttime (T able 1); these were combinedwith 85 previously ern NAapioidgenera toelev ated regions ofsimilar published ITSsequences (Downieet al. 2002), fora total of159 habitat,their similar life history and overall general accessions. Kartesz (1994), whose checklist ofApiaceae was inuenced by habit,and overlappingpatterns offruit variation sug- the workof Lincoln Constance,recognized 35 species of Cymop- gest thatthis group ofumbellifer smay beclosely re- terus inN A. Twospecies haveinfragenerictaxa: C. acaulis has ve lated. An obsolete stylopodium in allgenera save Pod- varieties; C. panamintensis has two. Withthe exception ofthe nar- istera,where the stylopodium is well developed asit rowlyendemic and rarelycollected C. megacephalus M.E. Jones,w e sampled all taxa of Cymopterus.Wealso included the recentlyde- is in most other umbellifers (Mathiasand Constance scribed C. constancei (Hartman 2000) and C. longilobus , the latter 1944–1945), is asynapomorphy uniting the group placed insynonymy under Pteryxia hendersonii byKartesz (1994) (Downie et al.2002). Further supportfor their mono- but maintained as adistinctspecies of Cymopterus byR. Hartman (unpubl. data). Followingthe checklist ofKartesz (1994), we sam- phyly comes from the shared presence ofa protogyn- pled all seven recognized taxa of Aletes (plus the Mexican A. cal- ousbreeding system (and associatedreproductiv eand cicola;Mathias and Constance 1981), bothsubspecies of Glehnia ecologiccharacteris tics),atypical in afamily where o- littoralis,and all seven taxa of Pteryxia (P.terebinthina var. calcarea ismaintained as distinctfrom P.terebinthina var. albiora, based on ral protandry prevails (Lindseyand Bell 1980;Lindse y Goodrich 1986). Allspecies of Musineon, Oreonana, Oreoxis, Oro- 1982;Barrie and Schlessman1987;Schlessman et al. genia, Podistera, Polytaenia, and Pseudocymopterus were also includ- 1990;Schlessman and Graceffa2002).
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