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Relationships Among the Spruces (Picea , Pinaceae)

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Relationships Among the Spruces (Picea , Pinaceae) SystematicBotany (2004),29(2): pp. 275– 295 q Copyright 2004by the AmericanSociety of PlantTaxonomists Relationships among the Spruces ( Picea,Pinaceae) ofSouthwestern North America F. THOMAS LEDIG,1,4 PAUL D. HODGSKISS,1 KONSTANTIN V. KRUTOVSKII,1 DAVID B. NEALE,1 and TEOBALDO EGUILUZ-PIEDRA2,3 1Institute ofF orest Genetics, Pacic Southwest Research Station,USD AForest Service,and Departmentof Environmental Horticulture,University ofCalifornia, One Shields Avenue,Davis, California95616; 2Centro de Gene´ticaF orestal, UniversidadA uto´noma Chapingo, ApartadoPostal N o.37, Chapingo, Me´xico, C.P.56230,Me ´xico; 3Present address: GrupoGenfor, Calle HuautlaN o.109, San Luis Huexotla,T excoco,Me ´xico, C.P.56230,Me ´xico; 4Author forcorrespond ence (e-mail:tledig@ucd avis.edu) CommunicatingEditor: Aaron Liston ABSTRACT. Numerous populationsfrom six spruce taxa, including four relict endemics, Picea chihuahuana (Chihuahua spruce), P.martinezii (Mart´‡nez spruce), P. mexicana (Mexican spruce), and P.breweriana (Brewerspruce), and twowidespread species, P.engelmannii (Engelmannspruce) and P. pungens (bluespruce), were compared athomologous isozymeloci totest various hypothesesabout theiraf nities and origins.Each ofthe species was clearly separated,and Neighbor-Joiningand UnweightedP air Group analyses ofN ei’s genetic distance grouped all populations withina taxon intotheir o wn clusters. Spruces fromFlys P eak, Chiricahua Mountains, Arizona, joineda P.engelmannii cluster and were nota bridgeto P. mexicana as previouslybeliev ed. Spruces fromCerro M ohinora, Chihuahua, were clearly P. mexicana,notphantom hybridsof P. chihuahuana and P. pungens.Nuclear randomampli ed polymorphic DNAand chloroplastsimple sequence repeat and cleaved amplied polymorphic genetic markerswere compared ina smallersample ofpopula tions, usingdistance and parsimony approaches. DNAmarkers,like isozymes, clearly identied spruces fromCerro Mohinora as P. mexicana.Incontradicti on to the mostrecent taxonomictreatment, P.chihuahuana and P.martinezii were separated as distinctspecies byboth isozyme and DNAmarkers,and formeda sister-speciesgroup. Picea engelmannii and P. mexicana formeda separate cluster, and the genetic distance between themwas similarto values associated withclosely related species but greaterthan distances typical of subspecies orv arieties inconifers. Picea pungens ,which isso similar to P.engelmannii thatthe twoare frequentlymisidentied, was clearly distinguishedfrom it, sometimesjoining a P.chihuahuana -martinezii group and sometimesa P.engelmannii -mexicana group,depending on analysis. Picea breweriana was well isolated fromall othertaxa. BothDN Aand isozymephylogeni es agreed withresults from crossability studies and contradictedintragenericrelationshipsconstructed largelyon cone mor- phology. Spruce (Picea A.Dietr .)is ataxonomicallydif cult 1988).The recent conifer checklist (Farjon 2001)rec- genus becausethe species encompass arelativelynar- ognized 34species, three subspecies, and 15v arieties, row range in morphology and ecologicalpreferenc e butconsidere d P.martinezii conspecic with P. chihu- (Wright 1955;T aylor and Patterson 1980;Rehfeldt ahuana Mart´‡nez(Chihuahua spruce). M ost species are 1994).T axonomists have encountered problems in de- Asian, and found predominantly in borealand cool limiting species and constructing phylogenies, and temperate or montane biomes. In Taiwanand Me´xico, early attempts atdividing the genus into sections and montane species extend south ofthe Tropic ofCancer . series were based on comparisons offew species (as Ofa totalten taxain North America, six occurin reviewed by Alde´n1987).Intragener icclassi cations the southwestern United Statesand Me´xico(Fig. 1). based on morphology (Bobrov1970; Schmidt 1989) Fourof the six are relicts, based on fossil evidenceor made implausible groupings when compared tothe biogeography,and are now rare endemics(W olfe 1964; results ofcontrolled hybridization, which are assumed Lozano-Garc ´‡a1993;Ledig et al.2000b); i.e ., P. marti- tore ect genetic similarities and differences. The sit- nezii, P.chihuahuana , P. mexicana Mart´‡nez (Mexican uationis complicatedby h ybridizationin areasof sym- spruce),and P.breweriana S.Wats.(Brew er spruce).In patry (Roche 1969;Bobrov 1970;Daubenmi re 1974; allof the three Mexicanspecies, trees number only in Taylor et al.1975; Gordon 1976b;Krutovskii and Berg- the hundreds tothousands (Ledig et al.2000b). Be- mann 1995;Rajora and Dancik 1999). causeof their rarity,few studies ofany kind have been Sprucesbelong tothe Pinaceae,and include 28to published on P.breweriana , P.martinezii , P.chihuahuana , 50species, dependingon the taxonomicauthority or P. mexicana. (Wright 1955;Everett 1981;Schmidt 1989).M ost tax- Piceapungens Engelm. (bluespruce) is more wide- onomists have acceptedabout 36 to 37 species (Bobrov spread than the endemic relicts. Itoccurs in the Rocky 1970;Schmidt-V ogt 1977;Rushforth 1987;Schmidt Mountains, primarily in Wyoming, Utah,Colorado , 1989),to which we would add Piceamartinezii T.F. Pat- and NewMexico,with disjunct outliers asfar north as terson (Mart ´‡nez spruce),described in 1988(P atterson northern Montana,as far w est asthe GreatBasin, and 275 276 SYSTEMATIC BOTANY [Volume 29 FIG.1. The natural distributionsof P.engelmannii , P. pungens, P.breweriana , P.chihuahuana , P.martinezii , and P. mexicana in westernNorth America (afterLittle 1971, Grifn and Critcheld 1976, and Ledig et al. 2000b), with location ofsampling sites used forDNA markers: P.chihuahuana (Ch), P.martinezii —Can˜on el Butano ( EB)and La Tinaja ( LT); P. mexicana—Sierra el Coahuilo´n( SC),Sierrala Marta ( SM),and CerroMohinora ( CM); Picea engelmannii (E); P. pungens (Pu); P.breweriana (Br). 2004] LEDIGET AL.: SPRUCEOF SOUTHWESTERNNORTH AMERICA 277 asfar south assouthern Arizona (Little 1971). Picea parently retreated northward during Holocene warm- engelmannii Parry ex Engelm. (Engelmann spruce)has ing. the widest range ofany species in the group,extending Botanists discovered P.martinezii in twolocationsin from the southernmost United Statesto northern Brit- the Sierra Madre Oriental in 1984,but reported the ish Columbia,Canada. Piceaengelmannii is predomi- discovery asnew records of P.chihuahuana (Mu¨ller-Us- nantly aspecies ofthe Rocky Mountains, butis also ing and Alan´‡s-Flores 1984;Mu ¨ller-Using and La¨ssig found on the east slope ofthe Coastand Cascade 1986).After further observation,P atterson (1988)de- Ranges through British Columbia,W ashington, and cided that P.martinezii wassuf ciently different from Oregon, southward toan outlier in the SiskiyouM oun- P.chihuahuana in needles, pulvini, and margins ofthe tains ofCalifornia, and on montane sky islands ofthe cone scales tonam eit anew species. More recently, GreatBasin (Little 1971). wehaverecorded afew new populationsof P. marti- Based on its distribution, P. mexicana appearsto be nezii (Ledig et al.2000b) in addition tothe original arelict stranded on the highest peaks ofthe Sierra Ma- discoveries byMu ¨ller-Using and Alan ´‡s-Flores (1984). dre Oriental and the Sierra Madre Occidental by Piceabrew eriana is arelict ofthe widespreadArcto- warming temperatures. Itoccurs at only three con- Tertiary ora,now conned toscattered ridges and rmed locations,on Sierra laMarta (3,500 m) and Si- north slopes in the western Klamath GeologicalProv - erra el Coahuilo´n(3,470m) in the Sierra Madre Ori- ince (Wolfe 1964;Grif n and Critcheld 1976;W aring ental and 676km awayon Cerro Mohinora (3,185m) 1969;W aring et al.1975). It has anorth-south range of in the Sierra Madre Occidental. Piceamexicana has been about220 km and outliers may occuras far as 150 km called avariety of P.engelmannii (var. mexicana (Mart´‡- from the Pacic coast.It is easily recognized by its nez)Silba) by Taylor and Patterson (1980).H owever, large cones and weeping habit. Webelieve thatmorphol ogy is not areliable guide others (A.G .Gordon, pers. comm.1988) felt thatthe torelationsh ips within Picea.For example,becauseof differencesbetween P. mexicana and P.engelmannii were the difculty in identifying P. pungens and P.engelman- sufcient towarrant their recognition asdistinct spe- nii when the twooccurin sympatry,widespreadh y- cies. The spruces on Cerro Mohinora remained prob- bridizationwaslong invoked,suggesting aclose rela- lematic forsev eral years afterthey were rst observed tionship (Habeckand Weaver 1969;Daubenmir e1972; by Correll (1960).The ywere popularlyknown as P. Taylor et al.1975). H owever, the cross proved difcult ‘‘indeterminada’’(J.Sa ´nchez-Cordovapers. comm. tomake ,and molecular datahas revealed no, or few, 1988) and P. ‘‘hybrida’’(Taylor and Patterson 1980),al- naturalh ybrids (Ernst et al.1990). Because ofthe dif- luding tothe confusion over whether they were phan- cultyin making controlled crosses between P. engel- tom hybrids of P.engelmannii with P. pungens and/or mannii and P. pungens,ahigh rate ofabnormaliti es in the local . occurs only P.chihuahuana Piceachih uahuana the hybrid progeny,and apaucityof natural h ybrids 57km awayfrom the spruces on Cerro Mohinora, but (Ernst et al.1990), P.engelmannii and P. pungens seem the nearest populationsof P. pungens are about780 km tobe good biologicalspecies in the sense ofMayr distant in southern Arizona.Initially ,Taylor and Pat- (1963). terson (1980)leaned toward ahybrid origin, butlater Piceabrew eriana and P. pungens have cones in the 6– consideredthe spruces from Cerro Mohinora conspe- 12cm range ,and P.chihuahuana and P.martinezii in
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