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236 ShortCommunications [Auk, Vol. 117

The Auk 117(1):236-241, 2000

A Preliminary PhylogeneticHypothesis for the (Cotingidae) Basedon Mitochondrial DNA

RICHARD O. PRUM,1 NATHAN H. RICE,2 JASONA. MOBLEY,3 AND WALTER W. DIMMICK NaturalHistory Museum and Department of Ecologyand Evolutionary Biology, University of Kansas, Lawrence, Kansas 66045, USA

The cotingas(Cotingidae) are a diversefamily of tion, but that a few generaof putativecotingids lack Neotropicalsuboscines that are thought to beclosely the derived condition, viz. Rupicola,, relatedto (Pipridae) and tyrant flycatchers Carpornis,, Ampelioides, cryptolophus, (Tyrannidae)in the superfamilyTyrannoidea (Lan- L. subalaris,and Oxyruncus. yon 1985;McKitrick 1985; Sibley and Ahlquist1985, Prum (1990)proposed a monophyleticCotingidae 1990;Prum 1990). The cotingas include species with on the basisof the sharedpossession of a derivedin- a great variety of plumages,breeding systems, and sertionof an extrinsicsyringeal muscle, M. tracheo- ecologies,and theyexhibit the largestrange in body lateralis, on the lateral membrane between the A1 size of any passerinefamily (Snow 1982). Under- andB1 syringeal supporting elements. This clade in- standingthe evolutionaryhistory of variationin cluded all of the cotingassensu Snow (1979),with thesetraits requires a corroboratedphylogenetic hy- the additionof Tityraand Phytotoma and with theex- pothesesfor the group. clusionof ,Pipreola, and Ampelioides.These Toward this goal, we have conducteda prelimi- family limits alsoleft Oxyruncusand the six genera nary molecularphylogenetic analysis to identifythe of the Schiffornisgroup (Prum and Lanyon1989) un- major cotingaclades and reconstructtheir interre- alignedwithin the tyrannoids.Subsequent morpho- lationships.Modern phylogenetic studies of the co- logicalobservations and a phylogeneticreanalysis of tingashave included five analysesof morphological the data supportthe inclusionof all of theseprob- and moleculardata. Somecotingas were includedin lematicgenera within a singlecotingid clade that in- phylogeneticstudies based on allozymeelectropho- cludesthe Cotingidaesensu Snow (1979), the Schif- resis (Lanyon 1985) and DNA-DNA hybridization forhis group, , and Phytotoma(R. O. Prum un- (Sibleyand Ahlquist 1985,1990; Sibley et al. 1985). publ. data). Furthermore,Prum (1990)performed a test of the Specifically,Pipreola and Ampelioideswere incor- monophylyof the cotingasbased on morphology. rectlycoded by Prum (1990);M. tracheolateralisin Prum and Lanyon(1989) did a phylogeneticanalysis Pipreolaand Ampelioidesinserts on both the lateral of the Schiffornisgroup based on morphology,and A1/B1 membraneand the A1 element (R. O. Prum Lanyonand Lanyon(1988) analyzedthe relation- unpubl.data). Thus, these genera share the derived shipsamong the genera of thePhytotoma group using stateof the cotingasand are membersof the morphologyand allozymeelectrophoresis. Here, we clade.Furthermore, the intrinsic syringeal muscles of analyzedata from sequencesof mitochondrialDNA the other problematicgenera (Oxyruncusand the from individuals of 32 cotinga speciesin 26 genera Schiffornisgroup) insert on the lateralA1/B1 mem- and 7 outgroup taxa. brane(Prum and Lanyon1989, Prum 1990).The in- Monophylyof cotingas.--Firstrecognized in nearly trinsicsyringeal muscles have evolved independent- its modernform by Sclater(1888), the Cotingidae has ly severaltimes within the cotingaclade (e.g. Lipau- variedsomewhat in taxonomiccomposition over the gus, excludingL. cryptolophusand L. subalaris,and last century (Ridgway 1907; Hellmayr 1929; Snow Procnias),and in eachinstance the intrinsicmuscles 1979,1982). Garrod (1876)first recognizedthe close insert on the lateral A1/B1 membrane, as does the relationshipbetween manakins and cotingasbased primitive undifferentiatedM. tracheolateraliswithin on the presenceof an enlargedfemoral artery. Prum (1990)established that the majorityof cotingasand the cotingaclade. Ample additionalevidence indi- manakinspossess thederivec( femoral artery condi- catesthat intrinsicsyringeal muscles are evolution- arily derivedfrom undifferentiatedM. tracheolater- alis (Ames1971, Prum 1992).Thus, good support ex- • E-mail: [email protected] ists for the hypothesisthat the intrinsicsyringeal 2Present address: Academy of Natural Sciencesof musclesof Oxyruncusand the Schiffornisgroup Philadelphia,1900 Benjamin Franklin Parkway, Phil- evolvedsubsequent to the derivationof the nearly adelphia,Pennsylvania 19103, USA. uniqueinsertion of M. tracheolateralison the lateral 3Present address: Department of IntegrativeBiol- membrane.Oxyruncus and the Schiffornisgroup also ogy, University of California, Berkeley,California are membersof the cotingaclade. 94720, USA. Becauseof apparent homoplasyin the derived January2000] ShortCommunications 237 femoral artery condition within the cotingas(see GenomicDNA wasextracted from eachsample us- above;Prum 1990), the monophylyof the cotingas ing Qiamp tissue-extractionkits availablefrom Qia- cannotbe strictlysupported on currentmorpholog- gen.The 3' endof the cytochrome-bgene (ca. 375 bp) ical data alone.However, the monophylyof this ex- was amplified using conventionalthermal-cycling panded cotinga clade can be supported assuming techniques,with a thermal profile of denaturingat that the absenceof the enlargedfemoral artery is a 95øCfor 30 s, annealing at 55øCfor 30 s, and exten- secondaryloss in Rupicola,Phoenicircus, Carpornis, Pi- sion at 70øCfor 90 s (Kocher et al. 1989). Extension preola,Ampelioides, Lipaugus cryptolophus, L. subalaris, time was lengthenedby 4 s eachcycle for 35 cycles. and Oxyruncus.This acceleratedtransition optimi- Cytochrome-bprimers (L-15507 5'-CCAGACCTCC- zationof thefemoral artery character is supportedby TAGGAGACCCAGA-3', H-15915 5'-AACTGCAGT- the DNA-DNA hybridizationdendrograms of Sibley CATCTCCGGTTTACAAGAC-3') were developedby and Ahlquist (1985, 1990) and by phylogenetichy- ShannonHackett (H and L refer to heavy and light pothesesbased on allozymes(Lanyon 1985). strands,respectively, and numbersindicate relative Threegenera of formerpiprids (Piprites, Neopelma, positionon referencechicken sequence; Desjardins and Tyranneutes)share the derived femoral artery and Morais 1990). Amplified product was purified characterwith manakinsand cotingasbut lack the on a low-melt (1%) NuSieve GTG agarose (FMC known synapomorphiesof either family (Prum BioProducts)gel electrophoresedfor 45 min at 85 to 1990).Thus, the currentresolution of thecotinga and 95 volts; bands containing target products were ex- manakinclades leaves the phylogeneticposition of cised from the gel, and DNA was recoveredusing thesethree basal heteromerousgenera unresolved. Qiaquick spin columns(Qiagen). Neopelmaand Tyranneutesare sistertaxa (Prum 1990), The purified PCR product was sequencedeither but the relationshipsof the Neopelma-Tyranneutesmanually on acrylamidegels with Promegacycle-se- cladeand of Pipritesto the cotingaor manakinclades quencing chemistry,or amplified using only one have not been resolved. primer (heavyor light) and sequencedwith an AB! Methods.--Freshlyfrozen or ethanol-preservedtis- Prism AutomatedSequencer (Model 310). The ther- sues(liver, heart, or muscle)were providedby the mal profile used was denaturing at 96øCfor 10 s, an- AmericanMuseum of Natural History (AMNH), the nealing at 50øCfor 5 s, and extensionat 60øCfor 4 Academy of Natural Sciencesof Philadelphia min, repeated for 25 cycles.Negative controlswere (ANSP), the LouisianaState University Museum of used at eachstep of DNA preparationto test for re- Natural Science(LSUMNS), and the Universityof agent contamination.All taxa were sequenceden- KansasNatural History Museum (KU) for 37 species tirely in both directions. of cotingasand relatedoutgroups. The speciesex- DNA sequenceswere inspected individually for amined, institutions, and tissue collection numbers quality and comparedwith the publishedGallus gal- are: rubrocristatus (LSU 7664); scla- lus sequence(Desjardins and Morais 1990). For the teri (LSU 3562); Rupicolaperuviana (LSU 19004);Rup- sequencescollected with the automatedsequencer, icolarupicola (LSU 7575);Phoenicircus nigricollis (LSU variationbetween species was comparedagainst the 2898); Pipreolaarcuata (LSU 7654); Pipreolachlorole- originalelectropherograms as a furthercheck on se- pidota(LSU 6989);Ampeliodes tschudii (LSU 5457);Co- quencequality. The datawere examined for possible tingacayana (LSU 2653);Porphyrolaema porphyrolaema site saturationby plotting pairwise comparisonsfor (LSU 6989); Conioptilonmcilhennyi (LSU 1416); Car- all ingroupand outgrouptaxa of the numberof tran- podecteshopkei (ANSP 2381); Xipholenapunicea (LSU sition and transversionsubstitutions against the Ta- 20833);Gymnoderus foetidus (LSU 9586);Lipaugus uni- mura-Nei geneticdistance that was calculatedusing rufus (ANSP 2399); Lipaugusfuscocinereus (ANSP MEGA (Kumar et al. 1993). 5039); Lipauguscryptolophus (ANSP 4445); Lipaugus The monophylyof the cotingaingroup was as- subalaris(ANSP 48784); Procniasalba (KU 1244); Ox- sumed based on the shared-derived insertion of M. yruncuscristatus (KU 220); Cephalopterusornatus (LSU tracheolateralisor intrinsicsyringeal musculature on 12300);Perissocephalus tricolor (AMNH uncataloged); the lateral membrane between the A1/B1 elements, Pyroderusscutatus (LSU 8137); Querula purpurata and assumingthe reversalof the enlargedfemoral (LSU 2785); Haematoderusmilitaris (KU 1348); Iodo- artery characterwithin the ingroup (seeabove). !n- pleuraisabellae (LSU 9553); Pachyramphusmarginatus group variation was rooted by outgroup comparison (LSU 2951);Pachyramphus versicolor (LSU 1702);S chif- with Neopelmachrysocephalum, Piprites chloris, and fornis major (KU 1426); Laniisomaelegans (ANSP the piprids (i.e. Piprafilicauda, Xenopipo atronitens, 1558);Tityra cayana(LSU 9604);Tityra inquisitor(LSU Machaeropterusregulus, and Machaeropteruspyroceph- 18568); Piprites chloris(KU 1415); Pipra fasciicauda alus). (KU 1138); Xenopipoatronitens (KU 1228); Machaer- The equallyweighted, unordered data set was an- opteruspyrocephalus (KU 1418);Machaeropterus regu- alyzed using 100 replicatesof PAUP3.1.1 with ran- lusstriolatus (KU 1043);Machaeropterus regulus regulus dom stepwiseaddition for startingtrees and with (KU uncataloged);and Neopelmachrysocephalum (KU the tree-bisection-and-reconnectionbranch swap- 1376). ping and MULPARS options in effect (Swofford 238 ShortCommunications [Auk,Vol. 117

1993).The numberof taxa was too large to employ lioides,and Oxyruncus(clade 3; Fig. 1). Clade3 is the the branch-and-boundalgorithm. Additional analy- sistergroup to a cladethat includesa diverseassem- seswere performedin the samemanner using 3:1 blage of "core cotingas"(clade 4; Fig. 1): Procnias; transversion-transitionweighting, successiveap- Cotinga;the other canopy-dwellinglowland forest proximation(reweighting characters in subsequent genera Conioptilon,Porphyrolaema, , Xiph- parsimony analysesbased on rescaledconsistency olena,and Gymnoderus;two separateclades of pihas indicesof charactersin the equally weightedanaly- (Lipaugussensu stricto, and the L. cryptolophus-L.sub- sis), removal of third-codonpositions, and removal alaris clade); and a well-resolved fruitcrow clade of third-codon transitions. (clade5; Fig. 1) that includesHaematoderus, Querula, Decay indices (Bremer 1988) for clades in the Pyroderus,Perissocephalus, and Cephalopterus. equal-weightinghypothesis were calculatedwith Decay(or Bremer)indices measure the numberof PAUP3.1.1 usinga commandfile that performed10 additionalevolutionary steps (ad hoc hypothesesof replicateheuristic searches, with random stepwise homoplasy)that are required before a clade is not addition,while enforcingthe reverseconstraint for supportedby the data (Bremer1988). Of the 30 re- eachof the resolvedclades in the mostparsimonious solvedingroup clades, 19 had decayindices of 1 and outputtree. Bootstrap values for the equal-weighting 11 had decayindices of more than 1 (Fig. 1). The hypothesiswere calculatedusing 100 bootstrapped Schiffornisgroup with Tityra and the core cotinga replicatecharacter sets with 10 random-additionse- groupeach had decayindices of 2, whereasthe Rup- quenceheuristic searches each in PAUP3.1.1. icolagroup has a decay index of 1. The best-sup- Results.--Ofthe 375 basessequenced, 339 unam- portedclades include the Ampeliongroup with 3; the biguousbases were availablefor all ingroupand out- Rupicola-Phoenicircusclade with 4; Lipaugus(exclud- group taxa for analysis.All sequenceshave been de- ing cryptolophusand subalaris)with 6; the Pipreola- positedin GenBank(accession numbers AF123612 to Ampelioides-Oxyruncusclade with 7; the Cephalopte- AF123650). These 339 bases included 204 variable rus, Perissocephalus-Pyroderusclade with 5; and the sites,160 of which were phylogeneticallyinforma- Carpodectes-Xipholenaclade with 8. Bootstrapvalues tive. The percentsequence divergence varied among for all but a few clades were less than 50%. the ingrouptaxa from 4.3%(Cephalopterus ornatus vs. Theseresults are consistentwith the hypothesis Perissocephalustricolor) to 25.7% (Carpodecteshopkei that Neopelmaand Tyranneutesconstitute the sister vs. Laniisomaelegans). Tamura-Nei distances were groupto the manakinclade of Prum (1990).Accord- calculatedfor all pairs of ingroup and outgrouptaxa. ingly,Piprites, or the pipridsincluding Neopelma and Graphs of pairwise comparisonsfor all taxa of Ta- Tyranneutes,could be the sistergroup to thecotingas. mura-Nei distances and the number of transition and We performed four other characteranalyses to transversion substitutions were made for all codon evaluatethe robustnessof the equal-weightinganal- positions,and for eachof the three codonpositions ysis to alternative models of molecular evolution. separately.These plots indicatedthat the relation- First,transversion substitutions were weighted three ship betweentransition and transversionsubstitu- times more than transition substitutions, and maxi- tions and overall sequencedivergence at all codon mum-parsimonyanalysis yielded sevenequally par- positionswas linear, implying that saturationin simonioustrees of length1,569. The majorityof the thesesequences was limited. phylogeneticrelationships within the strict-consen- The resultof theparsimony analysis of theequally sus tree were congruentwith the equal-weighting weighteddata was a singlephylogenetic hypothesis hypothesis.The main differenceconcerned relation- of length1,072, with a consistencyindex of 0.301and shipsof the Rupicolaand Schiffornisgroups. In the a consistencyindex excludingautapomorphies of strictconsensus of the 3:1 weightedtrees, the Rupi- 0.269(Fig. 1). The cotingaswere identifiedas mono- colagroup was split into the Rupicola-Phoenicircus phyleticif the networkwas rootedin any of the out- and the Pipreola-Ampelioides-Oxyruncusclades, with group taxa (i.e. it was unnecessaryto constrainthe unresolvedrelationships to each other and to the monophylyof the cotingasin the analysis).The tree Ampelionand corecotinga groups. In all of the seven included many resolvedclades that are congruent fundamental trees in the 3:1 weighting analysis, with traditionaltaxonomies and with previousphy- Schiffornisand Laniisomaformed a cladethat was ei- logeneticanalyses of morphologicaland molecular ther the sister group to the rest of the characters. group,or the sistergroup to the rest of the cotingas The most parsimonioustree (Fig. 1) placesthe excludingthe other Schiffornisgroup species.Most Schiffornisgroup genera (Prum and Lanyon 1989), otherdetails of the equal-weightinghypothesis were with the additionof Tityra,as the sistergroup to the supportedby the 3:1 weightinganalyses. The rela- restof the cotingas(clade 1). An Ampeliongroup that tionshipswithin the Schiffornisgroup genera dif- includesAmpdion and Doliornisis the sistergroup to feredbetween the two analyses,and the monophyly the remainingcotingas (clade 2; Fig. 1). Thenext lin- of the genusPipreola was supportedonly by the dif- eageincludes a Rupicola-Phoenicircusclade as the sis- ferential-weightinghypothesis. ter group to a lineage composedof Pipreola,Ampe- Second,in a successiveapproximation analysis we January2000] ShortCommunications 239

Arepelion rubrocristatus Clade 2 Dofforalssclateri Rupicolaperuviana 4 Rupicolarupicola Phoenicircusnigricollis Pipreola arcuata Glade 3 Pipreola chlorolepidota ? Oxyruncuscristatus Ampelioidestschudii Carpodecteshopkei punicea Gymnoderusfoetidus Lipauguscryptolophus Lipaugussubalaris Porphyrolaemaporphyrolaema Conioptilonmcilhennyi Cephalopterusornatus Perissocephalustricolor Pyroderus scutatus Querula purpurata Clade5 I-- Haematoderus militaris 2 Lipaugusunirufus Glade 4 Lipaugusfuscocinereus Cotingacayana Procniasalba Iodopleuraisabellae Laniisomaelegans Pachyramphusmarginatus Pachyramphusversicolor Clade 1 Schifforalsmajor inquisitor cayana Pipdtes chloris

Piprids(5 Species)

Neopelmachrysocephalum F•c. 1. The singlemost-parsimonious hypothesis for the phylogenyof the cotingasbased on equally weightedcytochrome-b sequences. The numbers above some lineages are the decay indices that are greater than 1; otheringroup clades have a decayindex of 1. The labeledclades (1 to 5) are referredto in the text. Thepiprid species include Pipra filicauda, Xenopipo atronitens, Machaeropterus regulus, and M. pyrocephalus. recodedthe characters(base weight = 1,000)based Rupicola-Phoenicircusclade was placedas the sister on their rescaledconsistency indices from the most groupto the largeclade that includedthe Ampelion parsimoniousequal-weighting tree. This resultedin group,the Pipreola-Ampelioides-Oxyruncusclade,and a similartopology that identifiedmany of the same the corecotingas. This topology was stable to addi- relationships,except that the relationshipsamong tionalreweighting after the firstanalysis. the Schiffornisgroup generawere different,and the Last,eliminating either all third-codonpositions, monophylyof the Rupicolagroup was not supported. or third-codon transition substitutions, resulted in ThePipreola-Ampelioides-Oxyruncus cladewas placed poorlyresolved ingroup relationships that contained asthe sisterto the corecotingas (where the Rupicola only a few clades,most of which appearedin the groupresides in the equal-weightingtree), but the equal-weightinghypothesis. 240 ShortCommunications [Auk,Vol. 117

Discussion.--Prumand Lanyon (1989) identified dependentidentification of these genera within a themonophyletic Schiffornis group including six gen- cladesupports the hypothesisthat the enlargedfern- era (Schiffornis,, Laniisoma, Iodopleura, Pa- oral artery was lost a singletime in the commonan- chyramphus,and Xenopsaris)based on morphological cestorof the Rupicolagroup and a secondtime in Li- characters. The current molecular data set lacks two pauguscryptolophus -L. subalarisclade within the core of thesegenera (Laniocera and Xenopsaris),but the cotingaassemblage. This resultfurther supportsthe other four generaare placedwithin a cladeon the conclusion that the absence of the derived hindlimb basisof theseindependent molecular data (clade1; arterycharacter in thesegenera is a secondaryloss, Fig. 1). However,the moleculardata alsoinclude Ti- and that the heteromerouscotingas and manakins tyrawithin this clade.Tityra was specifically exclud- constitute a clade. ed from the Schiffornisgroup on the basisof mor- The monophylyof a numberof generawas explic- phologicalcharacters (Prum and Lanyon 1989, Prum itly supportedin this analysis,including Rupicola 1990).However, Tityra was hypothesized to be close- andPachyramphus. These molecular data also confirm ly alliedwith Pachyramphuson the basisof othermo- Prum's(1990) hypothesis, based on morphology, that leculardata (Lanyon1985; Sibley and Ahlquist1985, the genusLipaugus as currentlyconstituted (Snow 1990).Both hypotheses essentially could be correctif 1979, 1982) is a polyphyletic assemblageof two Tityrais the sistertaxon to the Schiffornisgroup. clades.In all analyses,Lipaugus cryptolophus and L. These molecular sequencedata also corroborate subalarisform a well-supportedclade that is not the existenceof the Arepeliongroup, which was rec- closelyrelated to rest of the genusLipaugus, repre- ognizedby Lanyonand Lanyon(1988) on the basis sentedhere by L. unirufusand L.fuscocinereus. Two of syringealmorphology and allozyme data. Lanyon cotingagenera were hypothesized to be paraphylet- and Lanyon(1988) presented compelling molecular ic: Pipreola(including Oxyruncus cristatus) and Tityra and morphologicalevidence that Phytotoma and Zar- (including Schiffornis).However, the monophylyof atornisare closelyrelated to Ampelionand Doliornis, Pipreolaand Tityra are eachstrongly supported by sowe concludethat the thesegenera are alsowithin additionalmorphological and plumagesynapomor- the Arepelionclade identified here. Furthermore,our phiesthat werenot analyzedhere. The molecular ev- resultssupport the monophylyof a Rupicola-Phoeni-idence for their paraphyly presentedhere is not circusclade that was first suggested by Lanyon(1985) strongly supported. and is congruentwith morphologicaldata (R. O. Our resultsare not sufficientlycomplete to pro- Prum unpubl. data). posean entire phylogeneticclassification for the co- Thisphylogenetic hypothesis suggests close phy- tingas.However, the four main corroboratedclades logeneticrelationships among several groups of taxa couldbe recognizedas subfamiliesof the Cotingi- thathave been closely associated in pre-phylogenetic dae: classificationsof the family (e.g. Snow 1979). The Tityrinae (type genusTityra Vieillot 1816),includ- fruitcrowclade (clade 5; Fig. 1) differslittle in com- ing Tityra,Schiffornis, Laniocera, Laniisoma, Iodopleura, positionfrom the classificationof Snow(1979, 1982), Pachyramphus,and Xenopsaris; including four large-bodiedgenera (Haematoderus, Phytotominae(type genus PhytotomaMolina Perissocephalus,Pyroderus, and Cephalopterus)and the 1782), including Arepelion,Doliornis, Zaratornis, and smaller-bodiedQuerula, but excludingthe large-bod- Phytotoma; ied Gymnoderusthat traditionallyis a memberof this Rupicolinae(type genusRupicola Brisson 1760), in- group.Furthermore, the core-cotingaclade (clade 4; cluding Rupicola,Phoenicircus, Pipreola, Ampelioides, Fig. 1) includesa diversityof generathat havebeen and Oxyruncus;and consideredas closelyrelated within the family. Cotinginae (type genus CotingaBrisson 1760), in- Within the core cotingas,the closerelationship be- cludingCotinga, Conioptilon, Porphyrolaema, Carpodec- tweenCarpodectes and Xipholenathat was impliedby tes,Xipholena, Lipaugus (sensu stricto), Lipaugus cryp- traditional classifications(Snow 1979, 1982) was tolophus,L. subalaris,Gymnoderus, Procnias, Haemato- stronglysupported. However, the closerelationship derus,Querula, Perissocephalus, Pyroderus, and Cephal- traditionallysuggested between Cotinga and Porphy- opterus. rolaemais not supportedby thesedata. The other re- Eachof thesetaxa has appearedin previousclas- lationshipsamong the core cotingagenera are not sifications(Bock 1994). Future phylogeneticefforts stronglysupported and needto be confirmedby ad- shouldfocus on testingthe monophylyof these ditional data. cladesand further corroboratingthe interrelation- The molecularphylogenetic analysis identifies a shipsof the specieswithin them. cladeincluding Rupicola, Phoenicircus, Pipreola, Am- Acknowledgments.--Wethank Fred Sheldon pelioides,and Oxyruncus(clade 3). This clade is cor- (LSUMNS), Van Reinsen (LSUMNS), Frank Gill roboratedby independentmorphological data (Prum (ANSP), Leo Joseph(ANSP), GeorgeBarrowclough 1990).All five generalack the derivedenlarged fern- (AMNH), and Mark Robbins(KU) for accessto and oral artery conditionin an apparentreversal of the assistancewith frozentissue specimens. Without the synapomorphyof the cotinga-manakinclade. The in- effortsof thesecurators and the manydedicated field January2000] ShortCommunications 241

collectorswho have contributedspecimens to these LANYON,S. M., AND W. E. LANYON.1988. The sys- invaluable collections, this research would not have tematicposition of the ,Phytotoma. been possible.Shannon Hackett (Field Museum of Auk 106:422-432. Natural History) kindly provided the primer se- MCKITRICK,M. C. 1985.Monophyly of the - quencesthat shedesigned. We thankTerry Chesser, dae (Aves): Comparisonof morphology and Robert Zink, and three anonymousreviewers for DNA. SystematicZoology 34:34-45. commentson the manuscript.The researchwas sup- PRUM,R. O. 1990. A test of the monophylyof the ported by a grant from the University of Kansas manakins(Pipridae) and of the cotingas(Cotin- GraduateResearch Fund to ROP,a Frank M. Chap- gidae)based on morphology.Occasional Papers man Fund grant to NHR, and grants from the Na- of the Museum of Zoology of the Universityof tional ScienceFoundation to ROP (DEB-9318273) and Michigan No. 723. WWD (DEB-9629366). PRUM,R. O. 1992.Syringeal morphology, phylogeny, and evolution of the Neotropical manakins LITERATURE CITED (Aves: Pipridae). American Museum Novitates No. 3043. AMES,P. L. 1971. The morphologyof the syrinx in PRUM,g. O., AND W. E. LANYON.1989. Monophyly . Peabody Museum of Natural and phylogenyof the Schiffornisgroup (Tyran- History Yale University Bulletin No. 37. noidea). Condor 91:444-461. BOCK,W. J. 1994. History and nomenclatureof avian RIDGWAY, R. 1907. The birds of North and Middle family group names. Bulletin of the American America, part 4. Bulletin of the United States Museum of Natural History No. 222. National Museum No. 50. BREMER,K. 1988. The limits of amino-acidsequence SCLATER,P. L. 1888. Catalogueof the birds in the data in angiospermphylogenetic reconstruction. BritishMuseum (Natural History), vol. 14. Brit- Evolution 42:795-803. ish Museum, London. DESJARDINS,P., AND R. MORIAS.1990. Sequenceand SIBLEY,C. G., ANDJ. E. AHLQUIST.1985. Phylogeny gene organizationof the chickenmitochondrial and classification of the New World suboscine genome.A novel gene order in higher verte- (Passeriformes: Oligomyodi: Tyran- brates. Journal of Molecular Biology 212:599- nides).Pages 396-430 in Neotropicalornitholo- 634. gy (P. A. Buckley,M. S. Foster, E. S. Morton, R. GARROD,A. H. 1876. On some anatomical characters S. Ridgely,and E G. Buckley,Eds.). Ornitholog- ..a.:•t. •...... •r,• _•:•_ divisions• passer- ICal lvlonograpns l'•o. ine birds. Part I. Proceedingsof the Zoological SIBLEY,C. G., AND J. E. AHLQUIST.1990. Phylogeny Societyof London 1876:506-519. and classificationof birds. YaleUniversity Press, HELLMAYR,C. E. 1929. Catalogueof birds of the New Haven, Connecticut. Americas. Part 6. Oxyruncidae-Pipridae-Cotin- SIBLEY, C. G., S. M. LANYON, AND J. E. AHLQUIST. gidae-Rupicolidae-Phytotomidae.Publications 1985.The relationshipsof theSharpbill (Oxyrun- of the Field Museum of Natural History No. 266. cus cristatus).Condor 86:48-52. KOCHER, T., W. THOMAS, a. MEYER, S. EDWARDS, S. SNOW,D. W. 1979. Tityrinae, Pipridae, Cotingidae. PXXBO, F. VILLABLANCA, AND A. WILSON. 1989. Pages 229-308 in Check- of the Dynamics of mitochondrialDNA evolutionin world, vol. 8 (M. A. Traylor, Jr.,Ed.). Museumof : Amplification and sequencingwith Comparative Zoology, Harvard University, conservedprimers. Proceedings of the National Cambridge,Massachusetts. Academyof SciencesUSA 86:6196-6200. SNOW,D. W. 1982.The cotingas.Cornell University KUMAR, S., K. TAMURA, AND M. NEI. 1993. MEGA: Press, Ithaca, New York. Molecular Evolutionary Genetics Analysis SWOFFORD,D. L. 1993.Phylogenetic Analysis Using (1.01). PennsylvaniaState University, University Parsimony(PAUP), version3.1.1. Distributed by Park. the author. LANYON,S. M. 1985.Molecular perspective on high- er-levelrelationships in the Tyrannoidea(Aves). Received4 June1998, accepted22 April 1999. SystematicZoology 34:404-418. Associate Editor: R. M. Zink