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Molecular Phylogeny and Taxonomy of Malesherbiaceae Author(s): Karla M. Gengler-Nowak Source: Systematic Botany, Vol. 28, No. 2 (Apr.

- Jun., 2003), pp. 333-344 Published by: American Society of Plant Taxonomists Stable URL: http://www.jstor.org/stable/3094002 . Accessed: 07/04/2014 19:40
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(2003), 28(2): pp. 333-344 Systematic Botany ? Copyright2003 by the AmericanSocietyof Plant Taxonomists

MolecularPhylogeny and Taxonomy of Malesherbiaceae


KARLA M. GENGLER-NOWAK 2426 Cranford Road, Columbus,Ohio 43221 (kgengler@columbus.rr.com) M. Plunkett Editor: Gregory Communicating
ABSTRACT. Malesherbiaceae are an angiosperm alliedwithTumeraceae and Passifloraceae. Thefamily contains family 24 speciesin thesinglegenus, and is distributed in thearidAndesand coastaldeserts of Chile,Peru, and Malesherbia, are several there ofspeciesin thegenus, cohesive no subgenera or sections Argentina. Although morphologically groups havebeen recognized. A phylogeny forthefamily was reconstructed ITS sequence data usingparsimony, from implied successive and maximum likelihood and successive weights, approximations, analyses. Parsimony, implied weights, apalmost identical four cladesand one weakly clade. proximations yielded topologies having strongly supported supported Maximum likelihood in a topology resulted thesamefour wellsupported clades, analysis usingmodelTrNef+G showing buttherootmoved themonophyly tobreak ofthefifth clade.Thefour cladeseachcontain well-supported morphologically similar and thefifth cladealso showssomemorphological cohesion. Thefive cladesaremorphologically species, divergent and maybe recognized Fivesections, at thelevelofsection. ParvisAlbitomenta, Malesherbia, Cyanpetala, taxonomically aredescribed. A keyto thesections is provided. tella,and Xeromontana,

are an angiosperm Malesherbiaceae family closely relatedto Turneraceaeand Passifloraceae (Fay et al. in the ofthethree are centered 1997).The distributions relatives, of themembers but,unliketheir neotropics, Malesherbiaceae are xerophytes restricted to theAndes mountainsand the coastal desert on theirwestern flankin Chile,westernArgentina, and Peru (Fig. 1). Thisdesert coversmoredegreesoflatitude than region arid desert(Trewartha 1966),and any otherintensely Malesherbiaceae occur overa large portionof it. The is therefore ideal forthe studyof thebiogeogfamily whichuntilrecently has not raphyoftheentire region, in any detail(Rundelet al. 1991). been investigated Malesherbiaceae exhibita suite of morphological ofbothTurneraceae and Passicharacters reminiscent are characThe flowers of Malesherbiaceae floraceae. floraltube (probably of axial terizedby a prominent origin [A. Bernhard,Universityof Zurich, pers. and a coronaarise, whichtheperianth comm.])from a longandrogynophore, and a persistent Unperianth. the three styles are free and like in Passifloraceae, widelyspaced upon theovaryapex. The seeds ofMalack thearil characteristic of thefamily's lesherbiaceae The leaves of the oftendenselypubescent relatives. are almostalways ciliatewith glanMalesherbiaceae and mostspedularhairsexudingan oily, fluid, sticky In whichare oftenmultiple-lobed. cies have stipules, theseperennials additionto thesemorphological traits, are uniquein that they glycosides; producecyanogenic B are the dominant A and tetraphyllin tetraphyllin compounds(Spencerand Seigler1978). Fay et al. (1997) showedMaUsingrbcLsequences, related toTurneraceae, tobe mostclosely lesherbiaceae It is as the sisterto thesefamilies. withPassifloraceae ifMalesherbiaceae and Turneraceae unknown splitbeforeTumeraceaeradiated(i.e. Tumeraceaeare monoa highly phyletic)or if Malesherbiaceaeconstitute

modifiedbranch nested within Turneraceae.Given in South Americaand AfTumeraceae'sdistribution it seemsbiogeographically that rica,however, unlikely boththefamilies are monophyletic. Ravenand Axelrod that Tumeraceae becameestablished on (1974)contend bothcontinents Mathe Paleocene (65-45 mya). during lesherbiaceaeare almost certainlynot that ancient thatTurneraceae 2002a), suggesting (Gengler-Nowak may notbe monophyletic. Malesherbiaceae are littleknownoutsideof Chile. The first treatment ofMalesherbiaceae comprehensive was a traditional revisionby Ricardi (1967). In his Ricardirecognized27 species in a single treatment, Malesherbia R. et P. Phenetic analysesof a morgenus, phologicalcomplexof fourspecies indicatesthattwo ofthesespeciesare best treated as varieties (M. gabrielae and M. taltalina) and thata third(M. multiflora) is fromone of the varieties(Gengler-Nowak indistinct 24 species are recogtherefore, 2002b).In this study, nized. Althoughthereappear to be severalmorphologicallycohesivegroupsof species in the genus,Ricardi neither recognizednor erectedsectionsor subthisdiversity. generarecognizing of a hyThe focusof thisstudyis theconstruction of Malesherbiaceae using pothesis of the phylogeny theinternal transcribed spacerregions(ITS) ofnuclear is examinedin light ribosomalDNA. This phylogeny Five sections are described ofthefamily's morphology. of and thedistribution based upon theITS phylogeny traits. morphological
AND METHODS MATERIALS ofMafor 39 accessions was collected Sampling.Leafmaterial all 24 speciesand driedin silicagel (Table lesherbia representing was ofeachspecies than onepopulation more 1). Whenavailable, was generally not however, sampling, sampled;moreextensive intheir ofthespeciesand/or ofmany due to therarity feasible in thefield; DNA Fourspeciescouldnotbe located accessibility.

333

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while ITS-2(White et al. 1990)and themodified ITS-5, primers ITS 2 was amplified ITS-3(White et al. 1990)and usingprimers followed a hotstart theinitial ITS-4.The PCR reaction protocol: was 5 minat 95?Cfollowed which cycle by6 minat 72?C, during was addedto eachreaction and the volume time Taq polymerase twodrops ofmineral oil.Thenext reactions 30cycles cappedwith 1 minat50?C, of1 minat95?C, and 45 sec at 72?C. The consisted wasextended after extension (at72?C) segment by4 seceachcycle thefirst of 45 sec. A final extension of 5 minat 72?C segment thereaction. werepurified eiAmplification completed products in agarosegels (lx TAE)byelectrophoresis and subsequent ther from theagarose Amer(U.S.Bioclean, separation using glassmilk usshamCorp., filtration IL) orbycentrifugal Arlington Heights, filter tubes(Millipore Bedford, MA).ReingUltrafree-MC Corp., wereconcentrated cleanamplification forsecovered, products quencing. Manualsequencing ofthepurified, double-stranded ITS amplification was performed version 2.0 products usingtheSequenase terminachain (Amersham IL) dideoxy Corp., Arlington Heights, tionmethod withforward ITS-5and ITS-3and reverse primers ITS-2and ITS-4.The reaction that of followed primers protocol ofthesequences wasperformed Sangetal. (1994). Electrophoresis in6% acrylamide run Gelswere at1,500 gelsusing wedgespacers. mA until stainmigrated to theend of thegel (apbromphenol 2.5 hrs)and subsequently fixed in 10% aceticacid. proximately filter Theywerethendriedto 3-MMWhatman paperfor2 hrs vacuum under film before to KodakXARx-ray for one exposure to sevendays.The ITS regions oftwospecies, Malesherbia weberbaueri and M. turbinea, weresequenced seusingan automated due tomanual difficulties Genetics (Molecular quencer sequencing of theUniversity of Georgia Research Services, Athens, Facility GA). Data Analyses. Boundaries of the ITS regions weredeterminedusingsequences forthecodingrepreviously published to theITS regions gionsof18S,5.8S,and 26S adjacent (compiled et al. 1990).Sequences in Torres werealignedusingClustalW et al. 1994)witha 10-point a transition (Thompson gap penalty, a gap extension of0.05,and a 3-point preference, penalty preferenceforidentical bases.Minor manualadjustments to thecomwere madetomaximize thenumber ofinvariable puter alignment sites anddecrease the number ofindels. Most ofthese adjustments weremadewithin thefirst 50 base pairsofITS 1. of thedata set utilized NONA 1.6 (Goloboff Analyses 1993a), Pee-Wee 2.15(Goloboff andHennig86 Inpar1993b), (Farris 1988). wereperformed, simony analysisusingNONA,100 replicates ofMalesherbiaceae. FIG.1. Distribution 60 trees and usingtree bisection-reconnecholding per replicate tion. Further was notnecessary. Thesecommands were swapping also used in Pee-Wee, which thefit ofthecharacters on optimizes In Hennig86, successive implied weights. apmaterial ofthese herbarium as wellas the treeby their from was extracted species character was performed after conversion weighting of six other collected accessions additional in proximations speciespreviously numerical format. forpolymorIUPACsymbols caroliniana to therequired thefield. Freshleavesof theoutgroup taxa,Piriqueta wereconverted to unknowns for thisprocess, bydefault were collected of Tumeraceae, from and Turnera scabra green- phisms theportion ofmissing datato0.68%from 0.30%ofthe was chosen Thisfamily because Tumeraceae increasing plants. house-grown as missing data in all three Gaps are treated protaxon ofMalesherbiaceae as thesister havebeenimplicated (Fay data matrix. and polymorphic sitesare accepted by NONAand Peeet al. 1997)and becauseRicardi and grams, (1967)notedthatPiriqueta suchas a Wee. sharesomemorphological Malesherbiaceae characters, andbootstrap values were Jackknife, Bremer, support computed is a neotropical coronaand floral tube.Turnera regenusclosely forMacintosh 1996),NONA,and PAUP*4.0b2 New World latedto Piriqueta (Arbo1995).Theonlyother genera usingXac (Farris In thecalculation of thejackknife 1999),respectively. American andaretherefore (Swofford in Tumeraceae areCubanandcentral wereperformed withbranch values,10,000 replicates swapping taxa. moreunlikely sister addition Bremer sequences per replicate. supDNA Isolationand Sequencing. Depending upontheamount and fiverandom werecalculated for theconsensus ofthemost DNA extractions total ofmaterial werecarried outusing ports parsimonious available, from NONA.BecauseDavis (1995)found that Bremer CTABextraction a modified supprotocol (DoyleandDoyle trees large-scale values be inflated ifall thetopologies trees insuboptimal on CsCl/ethidium may bromide port 1987) withsubsequent purification andbecause itis computationally difficult after 1982)ora CTABminiprep (Palmer protocol Doyle havenotbeensearched, gradients all ofthese three runs were trees, DNAwas tocalculate andDoyle(1987)andCullings separate performed (1992). Miniprep-isolated to determine iftheresults are searched. Unnotpurified varyas moretrees byCsCl gradient. valuesacross runswouldsuggest that mostof oftheITS regions and inter- changing support Direct, amplification symmetrical havebeenexplored andthat thesupport values are outusingprimers ITS-4and ITS- thetopologies was carried 5.8Sregion vening overestimated. toSanget notegregiously In thesethree withITS-5modified runs, 2,502, et al. (1990), 5,502, 5 ofWhite according treesup to fivestepslonger werecalculated. ofDNA from Bootherbarium and 10,502 al. (1995).In a fewcases,amplification from so ITS 1 was amplified werecalculated "fast" was particularly difficult, material 5,000 replicates using using straps step-wise

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and sequencing, withGenBank No. (ITS 1/ITS2). All vouchers at OS used forDNA isolation TABLE1. Accessions are deposited unlessotherwise noted. R. 199,AF276343/AF276396 M. angustisecta HarmsKMG & Refulio M. ardens J.F. Macbr.KMG & Arakaki KMG & Arakaki KMG & Arakaki 184,AF276347/AF276400; 185,AF276337/AF276390; 187,AF276363/AF276416 M. arequipensis RicardiDillon, & Santisteban 58, AF276364/ 4793,AF276342/AF276395; KMG,Solas,& Cuadras Sagastegui, KMG & Cuadras AF276417; 182,AF276341/AF276394 M. auristipulata KMG 65, AF276365/AF276418 RicardiKMG 61, AF276366/AF276419; M. campanulata & Matthei RicardiRicardi, 1748,AF276330/AF276383 Marticorena, M. densiflora Phil.KMG 115,AF276378/AF276401 M. deserticola Phil.Dillon& Dillon6013,AF276323/AF276376; KMG 93, AF276349/AF276402 M. fasciculata D. Don KMG 151,AF276322/AF276375; 9803,AF276321/AF276374 Stuessy M. haemantha HarmsHutchinson 1278 (UC),AF276354/AF276407 M. humilis Poepp. KMG 190,AF276336/ var.parviflora KMG 106d, AF276335/AF276388; (Phil.)RicardiKMG 106c,AF276338/AF276391; & Baeza9883,AF276318/AF276371; 9892,AF276319/AF276372 Marticorena, AF276389; Stuessy Stuessy, M. lactea Phil.KMG 44, AF276324/AF276377; 9876,AF276317/AF276370 Stuessy M. lanceolata KMG 55, AF276328/AF276381; KMG 133,AF276351/AF276404; RicardiKMG 54, AF276327/AF276380; Stuessy 12809,AF276329/AF276382 KMG 36, AF276326/AF276379; KMG 155,AF276332/AF276385 M. linearifolia (Cav.) Pers.KMG 23, AF276331/AF276384; M. lirana 9814,AF276352/AF276405 Gay var.liranaStuessy 6312 (A),AF276353/AF276406 M. lirana KuntzeHjertling Gay var.subglarifolia Phil.var.obtusa M. obtusa KMG 119a,AF276334/AF276387 D. Don KMG 28, AF276325/AF276378 M. paniculata KMG 118,AF276339/AF276392 M. rugosa KMG 37, AF276333/AF276386; KMG 114,AF276340/AF276393; Gay var.rugosa M. scarlatiflora KMG 287,AF276359/AF276412; KMG & Romero 295,AF276357/ Gilg KMG 286,AF276360/AF276413; P 369,AF276358/AF276411 KMG & Roque KMG & Salvador 350,AF276356/AF276409; AF276410; M. splendens RicardiKMG 188,AF276350/AF276403 M. tenuifolia D. Don KMG 191,AF276344/AF276397; KMG 192,AF276346/AF276399; KMG 197,AF276345/AF276398 M. tocopillana RicardiDillon& Dillon5719,AF276320/AF276373 M. tubulosa KMG & Bedoya 362,AF276362/AF276415 (Cav.)J.St.-Hil.KMG & Roque354,AF276361/AF276420; M. turbinea 198,AF276367/AF276420 J.EMacbr.KMG & Refulio M. weberbaueri KMG 288,AF276355/AF276408 Gilg var.weberbaueri Urban Shore caroliniana 175,AF276315/AF276368 (Walter) Piriqueta Turnera scabra 150,AF276316/AF276369 Millsp.Shore

ifthese branches which et al. (2000)found to yield com- effect on theplacement oftheother Mort addition, longbranch bootstraps oftheoutgroup eachother. search. arenotattracting to a heuristic Therefore, sequences parable thecomplete was also employed Maximum likelihood paniculata) lineagefrom using PAUP*4.0b8 or the (M. linearifolia-M. data setswereremoved, withsubsequent 3.04 (Posadaand Crandall 1998). and theunambiguous 2001)and Modeltest (Swofford KMG369andKMG287, parsimony Two accessions ofMalesherbia analysis usingNONA. scarlatiflora, wereidentical to a wereremoved from thedatasetbecausethey KMG 350. ModelTest was implethird of thespecies, accession RESULTS should be apwhich modeland parameters to determine mented PAUP*. The The ITS regions of the 24 species in maximum likelihood Data. resulting analysis using plied Sequence like- recognized by Gengler-Nowak werethen used in a maximum modeland initial parameters (2002b) were successfor theaddition lihoodanalysis sequence, usingthe"asis"option and The aligned sequences amplified fully sequenced. treesfrom theNONA TBR,and one of the mostparsimonious The resulting treewas savedand the were 466 bp long with 175 informativecharacters.Abas a starting tree. analysis maximum likelihood anal- solute lengths of the combined ITS 1 and ITS 2 regions newparameters usedinthesubsequent untilthetreetopology stabiwas repeated ysis.Thisprocedure from 420 bp in the outgroups, Turnerascabra werethenused in a ranged of thefinal lized. The parameters analysis ardens and to 450 bp in Malesherbia caroliniana, a random likelihood maximum Piriqueta moreexhaustive analysis using withtenrepetitions. addition sequence (KMG 185), M. campanulata (Ricardi, Marticorena,and in which siteswithambig- Matthei1748), M. A seconddatasetwas constructed M. lirana var. subglabrifolia, densiflora, are whattheir effects to determine weredeleted uous alignments The and M. shortestsequence within 37). (KMG rugosa deleted dataset.Theeight on thecomplete (21 segments sequence oneequal- Malesherbiaceae was that of M. ardens (KMG 184), a short indel with more than eachcontained sites total) NONAwas per- which had 444 bp. Within the ingroup, indels of one analysis using Parsimony alignment. lyplausible be affected. howthetopology formed as abovetodetermine might were scattered. A few indels in the outis to three bases theingroup and theoutgroup between Becausethebranch on the groups were longer; in addition to scattered indels of usingACCTRANoptimizations long(104mutations very ononeofthelonger one to fourbases, there was one gap of 11 bases in the and theroot falls datasetinPAUP*) complete couldbe a source attraction in theingroup, branches longbranch outgroup not found in the ingroup. G+C content ofpotential 1978;Hendyand (Felsenstein problems phylogenetic ranged from 52.2% in M. ardens (KMG 185) to 61.9% noted and Siddall Huelsenbeck 1989; (1999) 1997). Whiting Penny scabra. ofthelongbranches should haveno in Turnera that ofeither theelimination

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in Malesherbiaceae calculated 10,502. This suggests that the numberof different Sequencedivergences withMEGA 1.0 (Kumeret al. 1993) using theKimura kindsof topologies in theset of treesup to fivesteps model were greatest betweenall acces- longeris relatively thatthe Bremer 2-parameter small,indicating sions of Malesherbiatenuifolia and M. paniculata supportvalues werenotgrossly overestimated. treeoftheparsimony Ma(10.00%). Divergenceswere zero betweenM. humilis In theconsensus analyses, var.parviflora accessions lesherbiaceae are brokeninto severalwell-supported 9892) and threeother (Stuessy of thatvariety (KMG 106c,106d,and 190); M. tocopil- clades (clades A, B, D, and E; Fig. 2) and one clade lana and M. ardens and M. with weak support (clade C; Fig. 2). Relationships (KMG 187),M. angustisecta thesecladesare poorly resolved. (KMG 58, Dillonetal. 4793);and amongM. amongspecieswithin arequipensis M. and M. zweberofPeruvian and extreme north(all accessions), splendens, Composedexclusively scarlatiflora baueri. Withinthe ingroup, onlya fewshortsections, ern Chilean species,clade E is subdividedinto two which were deleted foranalysisof an unambiguous clades. Clade El, with fourspecies,is strongly supdata set,were difficult to align due to thepresence of ported as monophyletic, but its sisterclade, E2, is indels.Divergences between theoutgroup and ingroup weaklysupported.This second clade is composedof between Malesherbia haemantha and threesmall clades; the reranged from41.99% to 54.02%; divergence Turnera scabra and Piriqueta caroliniana was 29.01%.De- lationshipsamong these components remain unrethe outgroup and ingroupse- solved.Clade E2 collapsed in theparsimony spite thesedifferences, analysis data. quences could be easily aligned by eye forapproxi- of thecompletely unambiguous halfthesequence. The remainderof the species is strictly Chilean. mately Phylogeny. Malesherbiaceaewere stronglysup- Weaklysupportedas sisterto the largelyPeruvian clade in all phylogenetic clade E is a relatively ported as a monophyletic large,strongly supportedclade ofthetwo analyses relativeto the limited outgroupsampling ofsevenspecies(clade D; Fig.2). The larger used here.Parsimony charac- lineagesin clade D (clade D2) showsMalesherbia camanalysisof informative tersof the equally weighteddata matrix and M. lanceolata as sistertaxa,but the relayieldedfour panulata shortest treesof 301 stepswitha consistency indexof tionships M. lirana, M. obtusa, and amongthislineage, 0.76 and retention index of 0.92 (Fig. 2). These trees M. rugosa are unresolved. Clade D2 also suffered some differ in two respectsonly.The (M. ardens-M. toco- loss of resolution when the 21 ambiguoussites were tur- removed(Fig. 2). The second lineage (clade Dl) conpillana)clade is sisterto the (M. auristipulata-M. clade in twotrees, whereasin theother twotrees tainsonlyM. deserticola and M. densiflora. binea) the(M. ardens-M. tocopillana) clade is sister to the(M. The sister clade (clade C) to clades D and E contains clade. The otherinconsis- only Malesherbia and M. lactea,which are arequipensis-M.tenuifolia) fasciculata lies in the(M. scarlatiflora-M. clade. veryweaklysupportedas a monophyletic tency weberbaueri) group by The twoaccessionsofM. tubulosa are either mostclose- two homoplasiouscharacters in the NONA analysis to theremaining taxain theclade, and in one treeof the Pee-Weeanalysis(Fig. 2). The ly relatedand sister or one oftheaccessionsfallswithin thepolytomy con- Malesherbia humilis to clade lineage(clade B) lies sister M. scarlatiflora, M. splendens, and M. weberbaueri. taining lineC+D+E, and the (M. linearifolia-M. paniculata) Two analyseswereperformed data. age (clade A) is sister to therestof thefamily. usingweighted The program Pee-Weegenerated two treesof greatest The maximumlikelihoodanalysis was completed fit(totalfit= 1,828.9). One (301 steps)was identical to using a data set withthetwo of threeidentical accesthemostparsimonious treesin whichthe(M. ardens- sions of Malesherbia removed. Analysisusscarlatiflora M. tocopillana) clade is sisterto the (M. arequipensis- ing Modeltest indicated thattheTrNef+Gmodel (TaM. tenuifolia) clade (Fig.2). The other Pee-Wee tree(302 muraand Nei 1993)bestfits thedata. The finalshape from thefirst in thatthetwoaccessions parameterderived fromthe iterative steps)differed analyses was ofM. lactea are paraphyletic withrespect to theacces- 1.441209.The treeresulting fromthe maximum likesions ofM. fasciculata, rather thansister to thisspecies. lihood analysis(Fig. 3) shows some differences from Successiveapproximations character was theparsimony trees.The two accessionsofM. auristiweighting also employed. This methodgenerated 384 trees.Like pulata a clade sister to M. turbinea, and,withcomprise thePee-Weetrees, thestrict consensustreealso placed in theM. humilis twoaccessions lineage, grouptogeththe (M. ardens-M. tocopillana) clade sisterto the (M. er.The (M. ardens-M. tocopillana) clade is sister to the clade. The (M. linearifolia- (M. auristipulata-M. arequipensis-M. clade. turbinea) tenuifolia) M. paniculata) clade collapsedin thistree.The remainMore significantly, thereare rearrangements of the der of the treewas identicalto the consensusparsi- relationships amongthemajorclades due to a change in theplacement + Turnera). of theroot(Piriqueta monytree. The Bremersupportvalues forthe treeswere constant sisterrelationship betweenMalesherbia and fasciculata across the threeruns,althoughthe numberof trees M. lactea is broken. Malesherbia lactea is sister to a clade was morethanquadrupledfrom M. fasciculata and all other ofMaaccessions 2,502to containing investigated

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2003]

GENGLER-NOWAK: PHYLOGENY OF MALESHERBIACEAE

337 Piriqueta Turnera

lOG

Cyanpetala

5/100/100

5/100/3100

~9

1~~1/63/63 ]
1 4/93/90 ^^M. 5/ 100/100 9 5/98/97 11 I 11/63/70 1

M. linearifolia linearifolia M. linearifolia M. paniculata M. M. humilis humilis humilis M. humilis M. humilis M.fasciculata M.fasciculata C M. lactea M. lactea M. densifiora M. deserticola D1 M. deserticola M. obtusa M. lirana v. lirana M. lirana v. subglab. M. rugosa rugosa M. rugosa D2 M. campanulata M. lanceolata M. lanceolata lanceolata M. lanceolata M. tubulosa M. tubulosa M. scarlatiflora M. scarlatiflora M. scarlatiflora M. scarlatiflora M. scarlatiflora M. splendens weberbaueri ^M. M. haemantha M. auristipulata M. auristipulata M. turbinea M. tocopillana ardens M. ardens M. M. ardens E2 M. arequipensis M. arequipensis M. arequipensis angustisecta M. tenuifolia M. tenuifolia M. tenuifolia

5/100/ 100 (B Parvistella Y^/ .Q.104 Alioet ?/ Albitomenta ,6\>

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100

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values treescalculated mostparsimonious thefour FIG. 2. Consensustreederivedfrom support byNONA. Dashes indicate names.The twoheavy-type and on theright ofless than50. Majorlineagesare marked side) and thesection (circled by letters arrowsindicatethe two clades whichcollapse in the consensustreeobtainedwhen ambiguoussiteswere removedand the OG = outgroup. identical. in NONA. The two consensustreesare otherwise data matrix topologically re-analyzed

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338

SYSTEMATICBOTANY

[Volume 28 0_____.223__ ~ I Piriqueta PG Turnera M. lactea 0.009 M. lactea ____ M. fasciculata 0.002 M. linearifolia

0.223 0.139 0.020I

Cyanpetala
0.502 Parvistella

0.002

o0.002 M. paniculata

M. linearifolia M. humilis
M. humilis

1- ' >>0.001

--------^^^ 0.022

-- IM. r 0.002 1-?00022 M. humilis


0.029 (P J__I --

humilis

M. humilis
M. densflora

57
0.005 ,< U*U14 .0 -0.014

0.002 0 007 0.017

0009

M. deserticola 1 0.002 M. deserticola M. obtusa -- - M. liranav. lirana M. rugosa M. rugosa M. rugosa D2 M. campanulata M. lanceolata M. lanceolata M. lanceolata M. lanceolata M. tubulosa M. tubulosa M. scarlatiflora M. scarlatiflora El M. scarlatiflora M. splendens M. weberbaueri M. haemantha M. auristipulata M. auristipulata M. turbinea M. tocopillana M. ardens M. ardens M. ardens E2 M. arequipensis M. arequipensis M. arequipensis M. angustisecta M. tenuifolia M. tenuifolia M. tenuifolia
M. lirana v. subglab.

Xeromontana / Xe/romontan

D2

0.017

0.002 0.008| 0.007 0.004

-0-002 0.009

0.002 0.004 0.014 0.002 ' 0.009 0.002 0.002

Malesherbia

0.018

0.70.0.028 0.002 0.028 00 0.007 0.002 0.005 00.010 0.0116 0.002

0.002

0.002

FIG.3. The treeyieldedby maximum likelihood themajorlineagesfound analysisusingmodelTrNef+G.Forcomparison, in theparsimony and on theright); sections are also labeled.Branch areindicated analysesare marked (circled byletters lengths below branches. Branches have a length ofzero.OG = outgroup. lackinga number

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in turn, M. is paraphyletic lata-M. lactea) lesherbia. Malesherbia lineageby placingtherootbetween fasciculata, The M. members. humilis linand the other taxa. to theremaining ingroup fasciculata therelationships The lackofdata concerning paniculata) among eage is sister to the (M. linearifolia-M. clade. the majorlineageslikelyplays a role in theseresults. and When the (M. linearifolia-M. ofMalesherbiafasciculata To explorethebehavior clade is repaniculata) M. lactea, which appear to be a source of instability, moved,the six characters the monophyly supporting forthe analyses were conductedin which either of clades B+C+D+E become synapomorphies parsimony one or theotherspecieswas deleted.In bothanalyses, family. The relationships amongthesemajorclades are whichcould easily thetwo speciesremainedsisterto clade D+E. supportedby veryfewmutations, of of therootand rearrangements Parsimony analysesof the completeand unambig- resultin movement the possible of only the out- the major clades, especiallyconsidering uous data sets with the elimination betweenthe outgroupbranch attraction group taxa each yielded fourtopologiesidenticalto long-branch branch.The results thoserecovered long M. fasciculata analysisof and the rather by theoriginalparsimony one ofthemajorfamily data set.Whenonlythe(M. linearifolia- ofsampling error thecomplete (byignoring the new topology; M. paniculata) however, topolog- lineages) may also be influencing lineagewas removed, of taxon theeffects et al. (1993) investigated data Lecointre resulted. ical rearrangements Usingthecomplete in- samplingand foundincomplete moved as sisterto theremaining set,M. fasciculata samples oftenyield and theremaining hypotheses.To investigate majorlineagesand M. lactea misleading phylogenetic group, morefullyusing parsimony Us- thesepossibilities a variety of relationships witheach other. formed analyconfidence was again sis, a data set whichresolveswith greater data set,M. fasciculata ing theunambiguous withM. lactea as sister to therelationships sisterto theingroup, amongthemajorlineagesofMaleshfalling is needed. erbiaceaeand theoutgroups taxa. theremaining Maximumlikelihood has been suggestedto be less (Huelsenbeck susceptible to long branch attraction DISCUSSION butsee Siddalland Whiting 1997,1998; 1999).Analysis likelihood of ofthedata usingmaximum As impliedby the family's againimplicates unique combination and M. lacteaas sources of toand in accordancewith Malesherbia characteristics fasciculata morphological between because the rootinserts other workers'conclusions(Ricardi 1967; Takhtajan pologicalinstability, sister to therestof 1980; Cronquist1981),the species of Malesherbiaceae thesespecies,withM. lactea falling of removalof either ofthefam- the family a monophyletic clade.The monophyly form (Fig. 3). Interestingly, would be best testedusing a data set in- thesespecies in parsimony analysisresultsin topoloily,however, to the fullparsimony and a moreslowly gies identical moregenerain Turneraceae analysis,suggestcluding taxa are noterroneously that these placed together ing evolving gene. attraction of the rootof Malesherbiaceae The placement 1999). (Siddall and Whiting may by long-branch instaindicatesthatthe greatest further inferences for This finding ofbiogeographical impacttheformation uncertainties. is due to rooting in thetopology The parsimony the family. analysesshow the rootto bility and parsimony likelihood Maximum fallbetweenthe (M. linearifolia-M. methods, then, lineage paniculata) of the as to the exactplacement The entire and therestof thefamily. however, are in disagreement family, thatthe root lies and root. All analyses agree, however, of autapomorphies, is defined by a large number oftherootis the among the Chilean taxa (clades A, B, C, and D) and it could be arguedthattheplacement or (M. the(M. linearifolia-M. either to the(M. linearifolia- involves resultoflongbranchattraction paniculata) clade. branch (Felsenstein M. paniculata) 1978; Hendy and fasciculata-M.lactea) the supporting Althoughthereare few characters 1997),whichis longrelative Penny1989;Huelsenbeck theingroup. Siddalland relationships within branches to mostother among the clades at thebase of the ITS clades A, B, D, and E each enjoyhighsupcan- phylogeny, (1999)notedthata pair oflongbranches Whiting each otherin a spurioustopologyifone of portvalues (Fig. 2). These clades also are morpholognot attract of theseclades (clade A) conThe first ei- icallydistinct. is absent.The analyseseliminating thosebranches These and M. paniculata. or the(M. linearifolia-M. theoutgroup ther linearifolia paniculata) tains Malesherbia and blue or have toof the sepals branchare equivocal.The stability purplepetals intensely species ingroup inconpology to the removalof the outgroupindicatesthat thatare verylarge comparedto the relatively are in paniclesatop the placementof the (M. linearifolia-M. paniculata) spicuous floraltube.The flowers taxais notmisleading. long, slender branches bearing shortlypubescent to other relative branch ingroup the of branch, leaves. These species are nativeto centralMediterraRemoval (M. linearifolia-M. paniculata) Chile. on the other hand, destabilized the relationships nean and semi-arid The second lineage (clade B; Fig. 2) containsonly among the major lineages enjoyinggood supportin humilis. This species is composed of five the parsimony analysisand brokeup the (M. fascicu- Malesherbia

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varieties(Gengler-Nowak over 11? Chile.Malesherbia whichis almosta cushion 2002b) distributed lactea, spein latitudealong the coast and in the pre-Andesof cies, has veryshortinternodes and spatulateleaves, are either from and the flowers or in few-flowered Chile,with some disjunctpopulationsreported solitary Province and racemes. The anthers and pollenare yellow. Its native (37?30'S)(Hunziker Neuquen,Argentina lies above 3,500m in the Andes of Chile and Espinar1967).These plants,whichdo not growtaller habitat than30 cm,producemultitudes of small flowers with Argentina. If thesespecies are sisterspecies,thelack whiteor pale lavender or blueperianth and molecular evidenceis probably partsand often of morphological floraltubes.The pedicels are bractless. after theevolution of greenish Stip- due to rapid divergence shortly ules may be obsolete, and the leaves and flowers are thelineage, to drastically different perhapsin response that this habitats. pilose.Maximumlikelihood analysesindicate a monophyletic clade withM. linearifolia The family's finalmajorlineage(clade E; Fig. 2) is speciesforms and M. paniculata. M. humilis is so di- largelyPeruvian, withonlythreespecies (Malesherbia Morphologically, fromthe otherspecies thatthereis as yetno tenuifolia, M. tocopillana, and M. auristipulata) in three vergent evidencefrom thatthesetwolineagesare separateclades nativeto extreme northern Chile. Inmorphology in this"Peruvian"clade are thepresence novations of verycloselyrelated. band of androecialtissuewherethe filaSpecies adapted to montaneand verydry desert a thickened habitats clade D (Fig. 2). ments becomefreeat theapex oftheandrogynophore comprisethewell-supported This lineage is differentiated fromothersby white and the appearanceof red and orangepigmentation. flowers withclearyellowin thethroat tinted rather thanglo(withthe Theirovariesare generally cylindrical which has pale blue bose, and the valves of theircapsules,whichextend obtusa, exceptionof Malesherbia flowers)and a pilose androgynophore and corona (the plesio- beyondand oftentearopen the perianth condition forthefamily is glabrous). The sev- at maturity, are elongated.The long, tubularshape, morphic en speciesofthisclade are separated intotwolineages. reddishhues, and exertedstamensand stylesof the Malesherbia deserticola and M. densiflora (clade D1) are flowersof many species suggest thatthese may be have been distinguished by having unequal, asymmetrically hummingbird pollinated;hummingbirds fusedwiththeleaf observed nearbushesofM. ardens shaped stipulesor stipuleslargely (K. Gengler-Nowak, blade and petiole.In clade D2, thestipulesof thefive pers.obs.). Two clades comprise the"Peruvian"lineage. speciesare obsoleteor reducedto smallflapsoftissue. Clade The coronas of this clade's species are veryshortor El (Fig.2) is composedofspecieshavinglong,tubular reduced to a thickband of tissue at the base of the flowers withconstricted throats and petalswithpilose abaxial and adaxial surfaces. The reddish-orange perianth. or The last clade of Chilean speciesin theparsimony yellowflowers are arrangedintodense racemesheld treecontains Malesherbia and M. lactea (clade erect on sturdystems. All fourhave relatively few fasciculata C; Fig. 2). Moleculardata weaklysupporttheir close branches, givinga candelabra-like appearanceto the and their as sisterto clades D plants.The ITS data failedto resolvetherelationships relationship placement + E. In the parsimony one or the among the fourspecies.Malesherbia analysesexcluding and M. splendens otherspecies,thespecies'sister in fact, have identical ITS sequencesto M. positionto clades D + weberbaueri, E remainsunchanged.The morphologies of M. fasci- scarlatiflora (KMG 350), even thoughthe threespecies culataand M. lacteaare verydifferent from other The addition to theITS data spe- are easilydistinguishable. cies of Malesherbia. Unlikeother have set ofmorphology or another Malesherbia, they gene,suchas matK, may leaves lackingstipules,and usually help elucidate therelationships entire-margined amongthesespecies. theseleaves lack prominent Fourgroupsof species comprise clade E2 (Fig. 2). glandularhairs.A purple hue oftentintstheir whiteflowers. Bothspecieshave Malesherbia and M. turbinea areplantswith auristipulata relative to plantsize, although blood-red long,slenderbranches flowers blackanthers and blackglanhaving those of M. lactea are sinuous and largely under- dular hairsliningtheapices of thepetals and sepals. of M. fasci- Theirflowers ground;the many long, slenderbranches are easily dislodged fromthe racemes. culata form a spherically shaped bush.Bothspeciesare The darkgreenleaves,whichhave broad,lobed stiphairs.Beyond ules, are also lined withblackglandular heavilycoveredwith white,tomentose hairs.Unlike these minorsimilarities, M. lacteaand M. fasciculata mostPeruvian M. auristipulata and M. turbinea species, sharefewotherfeatures. The internodes oftheslender have floral tubeswhichare widerat thethroat thanin branches ofM. fasciculata are verylong,and therather themiddleofthetube.Accessto thethroat oftheflowsmall leaves are ellipticto narrowly lanceolate.The er,however, is stillrestricted by thecorona,whichis ends of the branchesbear small flowers thanthefloral tube throat and whichforms arrangedin narrower racemesor dichasia whichare thencompressedinto a glossysheathexceedingthe lengthof the perianth. and pollenare blue.This This constriction of thethroat of theflower compactglobes.The anthers by a narsemi-arid of row coronain thislineageand by a narrowperianth speciesis nativeto thepre-Andean region

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in other Peruvian speciessuggeststhatitmaybe func- (22?05'S),is morecloselyallied to theshrubby species data clearly tionallyimportant, perhaps by promoting pollinator in clade El. The ITS and morphological or restricting access to the flower of theaffinspecificity by some supportRundelet al.'s (1991) assessment nectarrobbers. itiesof M. tocopillana. Of unknownaffinities withinclade E is Malesherbia Molecularand morphological data are equivocalrewhichclosely resembles M. auristipulata and gardingtherelationships haemantha, among thelineagesin clade M. turbinea withitsblood-redfloral blackpollen E2. The Malesherbia ardens clade shareswiththeM. autube, and anthers, and glandular hairsliningtheleavesand ristipulata clade a reddishcorona (althoughthe color Its corona is also relatively clade and moreorperianth. long, although is blood red in theM. auristipulata rather thangreat- angish-red in theM. ardens approximately equal to theperianth, clade) and thepresenceof it.UnlikeM. auristipulata and M. turbinea, a glandularhair at theapex of each petal.Supporting ly exceeding M. haemantha's leaves are deeply pinnatifid and sub- thecloserrelationship of theM. ardens clade to theM. tendedby lanceolate The sharedtraits are un- angustisecta clade is the presenceof shortsepals relastipules. usual forthefamily and suggestthatthethree tubemorethantwiceas tube,a floral species tiveto thefloral are closelyrelated, but thelack of molecular evidence long as wide, and the absence of a glandularhair at forsuch a relationship that M. haemantha the apex of each sepal. The moleculardata support may indicate of M. auristipulata and M. tur- either splitfromtheancestor placement, depending upon thetypeofanalysis binea of thelin- performed. Further evidence is necessary to resolve the veryearlyin theevolutionary history and M. turbinea are found relationships amongtheclades in thisdiverselineage. eage. Malesherbia auristipulata The monophyly ofclade E2 is weaklysupportedin near each otheron opposite sides of the Chilean-Peand maximum anallikelihood ruvianpoliticalborder;M. haemantha is a narrowen- theoriginal parsimony demiclivingabout500 km to thenorthwest. The dis- yses. This clade collapsesin analysesoftheunambigand no morphological traits tribution suggeststhatperhaps northern populations uous data set, however, of the species' ancestor evolvedin isolation, resulting have been foundto unitethelineages.Low confidence formonophyly of this clade may best be viewed as in theautapomorphies M. haemantha. defining of a rapid radiation Malesherbia M. arequipensis, and M. ten- supportforinference culminating angustisecta, in a of Peruvian a constitute clade characterized havdiversity lineages,each unitedby a uifolia by species characters. leavescovered suiteof unique morphological dissected, inghighly revolute-margined The phylogenetic here,while with white,tomentose presented hairs.When present, the stiphypothesis severalwell-supported majorclades thatare ules are also highly dissected.These plantsare small resolving lacks strongsupport at its distinct, in panicles,theplesiom- morphologically bushes bearingtheir flowers base and resolution at it Data are needed,theretips. condition of the The three are species orphic family. thataddress the relationships among the major also unusual in thatthey lack theintense floral fore, largely clades and related Use ofgenes species. among closely colorsofother speciesofclade E. Malesherbia arequipenthan test the relathat evolve more ITS could slowly alsis and M. angustisecta have greenish-white flowers, of the clades. The inclusion tionships among major thoughthe upper portionof the styleand the stigma theresoevolvinggenes mightimprove ofM. tenuifolia morequickly ofM. angustisecta are pink.The flowers withinthemajorclades. when exposed to sunlight; are pink-red partsofflow- lutionof relationships ers lyingon the groundor in the shade lack pigmenTAXONOMIC TREATMENT in the tation.The presenceof some pink coloration that lost this clade flowers ofall three Fourof the fivemajorlineages are well defined speciessuggests by a plesiom- both morphological rather thanretained mostcolorproduction and moleculardata. Taxonomic in addition, recognition Malesherbia of thelineageswould emphasizethemorarequipensis, orphiccondition. has losttheringofandroecialtissueat theapex ofthe phologicaldiversity Alamonggroupsof Malesherbia. floral tubechar- though the (M. fasciculata-M. and thelong,tubular androgynophore lactea) lineage is not of all the othermembersof the Peruvian strongly acteristic in theITS phylogas monophyletic supported and characters clade. a few it has morphological defining eny, ar- will thusbe recognized. Malesherbia at thelevelofsecThe last lineagein clade E2 contains Recognition whichbear theirorange-red tion is appropriate in this genus. Not only does this densand M. tocopillana, semi- avoid thecreation in dense,long racemesheld on sturdy, ofmanysmallgenera(and therefore flowers biof further but also the possibility The coronais deeplyand sharply new binomials), branches. decumbent workestablishesthe phylotoothed,and the leaves are lobed and coveredwith nomial changesif future and M. lacteadiffershared by these genetic positionsof M. fasciculata glandularhairs. The characteristics species led Rundelet al. (1991) to postulatethatthey entlythanthisstudy. are closelyrelated.Ricardi(1967) suggestedthatM. Description of Malesherbiaceae. Shrubs3 cm to 2 or erect,bearing branches a very rare endemic to Tocopilla,Chile m tall, semidecumbent tocopillana,

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sparselyto denselypubescentwith both simpleand and simple, sessileor glandularhairs.Leaves alternate with a shortpseudopedicel;abaxial and adaxial surfaces sparselyto denselypubescent, marginsusually lined with glandularhairs.Most species havingstipules,thesesimpleor dividedintoup to tenlobes,mara ragins lined with glandularhairs. Inflorescence a dichasium or solitary. ceme,panicle,or,rarely, Flowers perfect and actinomorphic, usuallysubtended bya pair of bracts.Floral tube 4-48 mm long and persistent;ten-nerved; funnelform, obconical,or campanulate; yellow,white,red, orange,or greenish; usually withwhitish oryellowhairs.Sepals densely pubescent 5 and 2.5-17mm long;white, dark red,orange, yellow, blue or purple,lightblue,violet,or greenish. Petals5 and 2-16 mm long; white,red, orange,yellow, dark blue or purple,lightblue,violet,or greenish. Corona

as longas, or shorter thanperianth, somethan, longer timesreduced to a raised band of tissue at base of white,lightyellow, perianth; orange,or red; margin erose.Androgynophore 1.5-13.5mm,withor without a ringofthickened tissuewherejoiningtheovary. Stamens 5, freeand arisingfrom the apex of theandroof the floral gynophore, extending beyondthe throat tube and corona.Anthers blue,or black,openyellow, to releasetricolporate ing longitudinally pollen.Ovary or conical;pubescent; globose,cylindrical, havingone locule and three carpels; placentation parietal and ovules many.Styles3, freeand arisingfromapex of ovary, extending beyondthe anthers. Capsule cylinor fusiform, often teardrical, tri-valved, campanulate, and coronaupon dehiscence. Seeds one ing perianth to many, lackingan aril,ovoid withpittedseed coat. The family contains one genus,Malesherbia.

KEY TO THE SECTIONSOF MALESHERBIA 1. Petalsdarkblueor purple; than floral erect perianth partsas longas or longer ............. 1. sect.Cyanpetala tube; plants 1. Petals orpale blueto violet; white, red,orange, floral tubelonger than yellow, erect or semidecumbent perianth parts; plants 2. Leafmargins leavesand stem entire; flowers completely white-tomentose; solitary, many-flowered racemes, or, globose rarely, in few-flowered racemes ................................................. 2. sect. Albitomenta 2. Leafmargins notcompletely leafand stem entire; orvelutinous; iftomentose, leavesdeeply pubescence hispid, pilose, pinnatisect or flowers or obconical; in racemes tubular, flowers or loosepanicles campanulate, 3. Shrublets tubefunnelform and often ('30 cm);floral constricted around theandrogynophore . 3. sect.Parvistella tightly 3. Shrubs leavesfinely (>30 cm),ifshorter, floral tubecampanulate, dissected; or broadly tubular, funnelform obconical, and expanded around androgynophore 4. Floraltubered,orange, or yellow; ifwhite or greenish, leavesalso finely + glabrous, pinnatisect; androgynophore a ring ofthickened tissue at thebase oftheovary; usually bearing or conical 4. sect. Malesherbia ovary cylindrical 4. Floral tubewhite, or light blue;leavesnever greenish, pinnatisect; ofthickandrogynophore piloseand lacking ring enedtissue; globose .......................................... 5. sect.Xeromontana ovary

1. Malesherbia sect. Cyanpetala Gengler,sect. nov. SpeciesIncluded-Malesherbia linearifolia (Cav.) Pers., Frutices 25-150cm alta ramislongisgracilibus er- M. paniculata D. Don. ectiscaule breviexorientibus; foliis lanceolatis vel inferioribus 23-120 mm longis,sti- 2. Malesherbiasect. Albitomenta pinnatisectis, sect. nov. Gengler, lateinfundibuliforpulis saepe lobatis;tubofloris Perennes tectus trichomatibus albistomentosis rami coloreinconspicuo; tubumfloris aeperianthio mis graciles; foliorum trichomamargine integro vel atropurpuquantia vel longiore, atrocyaneo tibusglandulosisvulgo deficientibus; tubo floris M. linearifolia reo.-Typus hic designatus: (Cav.) minusquam 1.2 cm, albo interdum tincto violaPers. M. lactea Phil. ceo.-Typushicdesignatus: Shrubs 25-150 cm tall with long, slender,erect branches arisingfroma shortstem.Leaves lanceolate or pinnatisect, 23-120 mm long,stipulesoften lobed. Floral tube broadlyfunnelform, colinconspicuously ored; perianth equal to or longerthanthefloral tube, darkblue or darkpurple.The darkblue or purplehue is unique in the family, and the section's name was chosento reflect thistrait. Nativeto Chile (RegionsIII, IV,V,VI, VII, and Mein the northof its range,it is largely tropolitana); foundin theAndeanfoothills. In thesouth, thesection Ricardi(1967) ranges fromthe coast to the foothills. noteswithsome doubttheclaim thatM. linearifolia is native to Argentina;Hunziker and Espinar (1967) foundno confirmation in thatcountry. foritspresence Perennials covered withwhitetomentose hairswith branches leafmarginsentire, slender; glandularhairs usually lacking;floraltubes less than 1.2 cm long, white and sometimesviolet-tinted. The section is named forthewhitehairscovering bothspecies. Nativeto above 3500 m in the Andes of Chile (RegionsII, III, and IV) and adjacent Argentina (Provinces La Rioja and San Juan).Also foundin the semi-arid, foothills ofChileanRegionsIV,V,VI, and pre-Andean Metropolitana. Included-Malesherbia lactea M.fasciculata Species Phil., D. Don. 3. Malesherbia sect.Parvistella sect.nov.FruGengler, ticuli erecti ad 30 cm alta;foliis vulgoramosissimi

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lanceolatis vel oblongis, pilosis, pinnatisectis, ciliato trichomatibus glandulosis,infermargine interdum dificienioribus vulgo marcidis; stipulis 4-12 mm tubo floris tibus;pedicellisebracteatis; (2.0-6.5mmcircumlongis,0.5-2.0mm diametro infundibuliformi, virello,dense piloso, ferentia), faucenunquamtinctaflava;perianthio albo, caeraropiloso.lestivel violaceo; androgynophoro hicdesignatus: M. humilis Typus Poepp. 30 Shrublets branched, erect,oftenhighly reaching or oblong, cm in height; leaves pinnatisect, lanceolate, pilose, margins ciliate with glandular hairs, lower sometimes leavesoften withered, pedstipules lacking; floral tube4-12 mm long,0.5-2.0mm icelsebracteate; in diameter(2.0-6.5 mm in circumference), funnelnever tinted with form, densely greenish, pilose,throat blue,or violet;androgynwhite, yellow;perianth light ophorerarely pilose.The perianth partslie perpendicular to thefloral tubeoftheflowers, themany lending diminutive on a plant a star-like flowers appearance. name was chosenforthisfeature. The section's Nativeto thecoast and thepre-Andes ofChile from Santiagoto Guatacondo(20056'S)(RegionsII, III, IV,V, and Metropolitana). Also foundin the northof Province Neuquen (37030'S)of Argentina. humilis Included-Malesherbia Species Poepp. 4. Malesherbiasect. Malesherbia,sect. nov.- Typus: M. tubulosa (Cav.) J.St.-Hil.

flava; corona interdumdiminutainstarporcae; albo vel rarocaelesti, perianthio androgynophoro M. densiflora Phil. piloso.-Typushicdesignatus: and erect or semidecumShrubs, many-branched bent; leaves densely pubescent;stipules lacking,reduced, or asymmetrically shaped; floraltube funnelwiththroat oftentintedyellow; form or campanulate white coronasometimes reduced to a ridge;perianth or rarely pilose. pale blue; androgynophore in montane and verydrydesert habitats Distributed and of Chile (RegionsII, III, IV,V,and Metropolitana) La Rioja,Menextreme western (Provinces Argentina The section's name redoza, Neuquen,and San Juan). thehabitats of its constituent flects species. Included-Malesherbia Ricardi, M. campanulata Species M. deserticola Ricardi, Phil.,M. lanceolata Phil., densifora M. lirana Phil.,M. rugosa Gay. Gay,M. obtusa
I thankD. J.Crawford, A. Wolfe, K. ACKNOWLEDGEMENTS. and T. Stuessy fortheir comments, Pickett, help,and adviceand material for theoutS. Barrett andM. Cruzanfor plant providing I am grateful to J.Wenzelforuse of his copiesof the groups. and Hennig86 and hismany hours of NONA,Pee-Wee, programs withtheseprograms and to J.Freudenstein forhelp assistance a secondreviewer, withLatin. The comments of LeighJohnson, and Gregory Plunkett themanuscript, for which greatly improved I thank them. I am indebted to thefaculty and staff ofthefollowUniversidad de Concepci6n, theMuseoNaChile; inginstitutions: in Santiago, cionalde Historia Natural de Chile;theUniversidad La Serena, Natural Prado" in "Javier Chile;theMuseode Historia inArequipa, theUniversidad Nacional de SanAgustin Peru; Lima, in de Huamanga Nacional de San Cristobal Peru;theUniversidad inMoquegua, andthe theMuseoContisuyo Peru; Peru; Ayacucho, del Peruin Huancayo, Peru.I Nacionaldel Centro Universidad thank Naturales theInstituto Nacional de Recursos (INRENA)of to collectand export from that Peru forpermission specimens I further thank thefollowing herbaria for theloanofspeccountry. forthisstudy: imens ofMalesherbia A, CONC,CTES,F,GH, MO, conducted MOL,NY,SGO,UC,ULS,US, and USM.Thisresearch, Diswas funded at The Ohio StateUniversity, by NSF Doctoral theTinker Grant sertation Foundation, DEB-9623496, Improvement andSigma theBeatley Herbarium theFlora ofChileproject, Grant, Xi Grants-in-Aid ofResearch.

Shrubs with branches erect or semidecumbent; or deepleaveslanceolate, oblanceolate, oblongo-ovate, ly pinnatisect, denselypubescent;floraltube tubular white or obconical, red,orange,or sometimes yellow, or pale green;corona usually exceedingor equaling usuallyswollenat thebase perianth; androgynophore or conical. of theovary;ovarycylindrical broad Nativeto thearid,deep inter-Andean valleys, of Peru (Departvalleys,coast,and Andean foothills mentsArequipa,Ayacucho, Huancavelica,Ica, Junin, Lima, Moquegua, and Tacna). Also foundin the scatLITERATURE CITED tereddryriver valleysoftheAtacamaDesertofnorthParte I. Piriqueta. Flora M. M. 1995. Tumeraceae Chile(Re- ARBO, ernChileand alongthecoastnearTocopilla, Neotropica. New Botanical 67.TheNewYork Bronx, Garden, Monograph gionsI and II). York. Included-Malesherbia Harms,M. CRONQUIST, angustisecta Species Anintegrated A.1981. of classification system offlowering M. arequipensis ardens Ricardi,M. auristiJ.F Macbr., New York, NY. Columbia Press, University plants. PCR ofa plant-specific K. W.1992.Designand testing Harms, M. scarlatifloraCULLINGS, pulata Ricardi,M. haemantha studies.Molecular and evolutionary forecological primer D. Don, M. toM. tenuifolia Ricardi, Gilg,M. splendens 1: 233-240. Ecology M. turM. tubulosa Ricardi, (Cav.) J.St.-Hil., copillana the for I. 1995. structure A phylogenetic DAVIS,J. Monocotyledons, weberbaueri F. M. binea Macbr., Gilg. J. sitevariation, DNA restriction from as inferred chloroplast
20: 503-527. Botany sect. nov. 5. Malesherbiasect. Xeromontana Gengler, 1987.A rapidDNA isolation procevel semidecumbentes; DOYLE, J.J.and J.L. DOYLE. erecti Frutices ramosissimi material. leaf offresh durefor small Phytochemical quantities foliisdense pubescentibus; stipulisdeficientibus 19: 11-15. Bulletin infun- FARRIS, J.S. 1988.Hennig86 tubo floris vel redactisvel anisomorphis; Port 1.5.MS-DOS program, version NewYork. fauce vulgo tincta dibuliformi vel campanulato, Jefferson, ofclade support. ofmeasures and a comparison Systematic

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. 1996. M. 1967.Revisi6n taxon6mica de las Malesherbiaceas. RICARDI, Parsimony jackknifing outperforms neighbor-joining. Botanica. No. 16:1-139. 12:99-124. Cladistics Gayana P. W.,M. O. DILLON, B. PALMA, H. A. MOONEY, S. L. M. E, S. M. SWENSEN and M. W. CHASE. 1997.Taxonomic RUNDEL, FAY, and J.R. EHLERINGER. 1991.Thephytogeography GULMON, affinities ofMedusagyne Kew (Medusagynaceae). oppositifolia and ecology of thecoastalAtacama and Peruvian deserts. Bulletin 52: 111-120. Aliso13: 1-49. or compatibility FELSENSTEIN, J.1978.Cases in which parsimony and T E STUESSY. S.-C.KIM, 1994. RaT.,D. J.CRAWFORD, will be positively methods misleading. Systematic Zoology SANG, Dendroseris diation oftheendemic on the (Asteraceae) genus 27: 401-410. evidence from Fernandez Islands: oftheITS Juan sequences K. M. 2002a. Reconstruction of the biogeoGENGLER-NOWAK, of DNA. nuclear ribosomal American ofBotJournal regions ofMalesherbiaceae. The Botanical Review history graphical any81: 1494-1501. 68: 171-188. and T. E STUESSY. 1995.ITS sequences , D. J.CRAWFORD, --. 2002b. Phenetic ofmorphological inthe traits Maanalyses and thephylogeny ofthegenus Robinsonia (Asteraceae). Syslesherbia humilis Taxon51: 281(Malesherbiaceae). complex tematic 20:55-64. Botany 293. 1999.Long-branch abstracSIDDALL,M. E. and M. E WHITING. P. A. 1993a.NONA,version 1.6. MS-DOS program. GOLOBOFF, tions. Cladistics 15:9-24. Published the San de by author, Miguel Tucuman, Argentina. SPENCER, K. C. and D. S. SEIGLER. 1978. of Cyanogenic glycosides --. 1993b. Pee-Wee version 2.15.MS-DOSprogram. Published Malesherbia. and Ecology Biochemical 13:23-24. Systematics San Miguelde Tucuman, bytheauthor, Argentina. D. L. 1999.PAUP*. SWOFFORD, Phylogenetic Analysis UsingParM. D. and D. PENNY. 1989.A framework thequantifor HENDY, 4. Sinauer Version Associates, (*andOther Methods). simony tative trees.Systematic studyof evolutionary Zoology38: MA. Sunderland, 297-309. 2001. PAUP*.Phylogenetic AnalysisUsingParsimony zone a fly 4. Sinauer HUELSENBECK, (* and Other Version SunJ.P. 1997.Is theFelsenstein trap? SysAssociates, Methods). tematic 46: 69-74. MA. derland, Biology A. L. 1980.Outline oftheclassification offlowering . 1998. biasinphylogenetic is theStrep- TAKHTAJAN, Systematic analysis: Botanical Review solved? 47: 519-537. 46(3):225-359. plants (Magnoliophyta). siptera problem Systematic Biology K. and M. NEI.1993. Estimation ofthenumber ofnucleA. T. and L. A. ESPINAR. 1967.Notaaclaratoria sobre TAMURA, HUNZIKER, in the control otidesubstitutions of mitochondrial region las Malesherbiaceae y una clavepara su identifiargentinas DNA in humans and chimpanzees. Molecular and Biology 4: 83-86. caci6n. Kurtziana Evolution 10:512-526. and M. NEI.1993. MEGA:Molecular evoKUMER, S., K. TAMURA, and T. J.GIBSON. 1994.Clustal J.D., D. G. HIGGINS, 1.0. The Pennsylvania THOMPSON, version lutionary genetics analysis, W: improving of progressive the sensitivity semultiple State PA. Park, University, University quence through alignment sequence weighting, position speH. L. V.LE,and H. LEGUYADER. 1993. LECOINTRE, G.,H. PHILIPPE, cific and weight matrix choice. Nucleic Acids gap penalties has a major on phylogenetic inferSpeciessampling impact 22: 4673-4680. Research and Evolution 2: 205-224. ence.Molecular Phylogenetics G. T. 1966.The Earth's climates. The UniTREWARTHA, problem M. E., P. S. SOLTIS, D. E. SOLTIS and M. L. MABRY. 2000. MORT, ofWisconsin Wisconsin. Press, Madison, versity ofthree methods for internal Comparison estimating support TORRES, R. A.,M. GANAL, and V.HEMLEBEN. 1990. in GC balance on phylogenetic trees. 49: 160-170. Systematic Biology theinternal transcribed ITS 1 and ITS 2 ofnuclear spacers Isolation and structural ofchloroplast PALMER, J.D. 1982. analysis ribosomal RNA genes.Journal of Molecular Evolution 30: DNA. Nucleic AcidsResearch 10: 167-186. 170-181. D. and K. A. CRANDALL. 1998.Modeltest: the WHITE, POSADA, testing T.J., T. BRUNS, and J.TAYLOR. S. LEE, 1990. Amplification modelofDNA substitution. Bioinformatics 14:817-818. and direct of fungal ribosomal RNA genesfor sequencing P. I. H. and D. AXELROD. 1974. RAVEN, Angiosperm biogeography inPCRprotocols: A guide tomethods phylogenetics. Pp.315-322 and pastcontinental movements. Annals oftheMissouri Boandamplifications, D. Gelfand, eds.M. Innis, andT. Sninsky, J. tanical Garden 61: 539-673. White. San Diego,CA: Academic Press.

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