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Phylogenetic Relationships Among the Trogons

Phylogenetic Relationships Among the Trogons

The Auk 115(4):937-954, 1998

PHYLOGENETIC RELATIONSHIPS AMONG THE

ALEJANDRO ESPINOSA DE LOS MONTEROS• Departmentof ,American Museum of NaturalHistory, Central Park West at 79 Street, New York, New York 10024, USA

ABSTRACT.--Theorder Trogoniformescurrently is divided into six genera:, ,Euptilotis, , , and .For this study,the questionof in- tergenericrelationships was addressedbased on mitochondrialcytochrome b and 12S ri- bosomalRNA genes.Maximum parsimonyanalyses confirmed the monophylyof currently acceptedgenera. A monophyleticclade encompassing the New Worldgenera was the sister groupto the Asiangenus Harpactes. The sistergroup of theseclades, in turn,was the African genusApaloderma. Within the New Worldclade, the sistertaxon of the genusTrogon was a cladeformed by the EaredTrogon (Euptilotis neoxenus) and the (Pharomachrus spp.). The most basalgenus within the New World cladewas Priotelus.These results suggest an Old World (/Eurasia) for trogons,with the New Worldrepresenting a second- ary areaof diversification.Patterns in plumagecoloration concurred with relationshipsin- ferred from the moleculardata. A hypothesisfor the evolutionof iridescentstructures in trogonfeathers suggests an increasein the complexityof thesestructures in the youngest lineages.Received 7 July 1997, accepted 12 March1998.

THE TROGONSAND QUETZALS( Trogon- Morphologicalfeatures said to be character- iformes)are amongthe mostcolorful of . istic of trogons and quetzals (Ridgway 1911, They have dense,lax plumageand a well-de- Sibley1955, Sibley and Ahlquist1990) include veloped aftershafton their contourfeathers. a schizognathouspalate, basipterigoid process- The colorpattern of malesis brown or metallic es, a large vomer, 15 cervical vertebrae,two greenwith a blue-greengloss on the dorsalre- pairsof deepsternal notches, four to five pairs gion,and the headcan be metallicgreen, black, of ribs, a metasternumwith four notches,sep- gray, blue, violet, chestnut,pink, or red. In arated coracoids,a tracheo-bronchialsyrinx, manyspecies, the upperpart of the chestis sep- holorhinal nostrils having an ossifiednasal aratedfrom the lowerpart and the belly by a septum, Gadow'stype VIII deep plantar ten- conspicuouswhite band.The lowerchest, belly, don arrangement, intestinal convolutionsof and undertail covertscan be red, yellow,or or- type VI (Gadow 1889), pelvic muscleformula ange.The wingsare completelyblack, and the AX (Garrod 1873), a well-developedcaecum, tail is black with very distinctivepatterns of left carotid artery only, a well-definedspinal white.Some have colored bare periocu- pterila extending from the nape to the oil lar skin with tonalitiesranging from light yel- gland, 10 primaries, 11 to 12 secondaries,12 low to deeppurple. The quetzals (Pharomachrus rectrices, and an unfeathereduropygial gland. spp.) are characterizedby having a crested All of these features, however, also are found head, elongatedupperwing coverts,and up- in various combinationsin other groups of pertail covertsexceeding the lengthof the tail, birds (Sibleyand Ahlquist1990). Perhaps the which,in the ResplendentQuetzal (P. mocinno) only characterthat differentiatestrogons and can reach up to 70 cm. The bill is short but quetzals(hereafter trogons) from other groups broadbasally, usually brightly colored,has a is their heterodactylfoot in whichdigits 1 and stronglyarched culmen, and, in severalspecies, 2 are directed backward and digits 3 and 4 are has a serratedmaxillary tomium. The longtail united for their half and directed for- is graduated,broad at the base,and truncated. ward. The trogonsare widely distributedin the •Present address:Departamento de Ecologfay tropicsof both the Old and New Worlds.Sibley ComportamientoAnimal, Institutode EcologfaA.C., and Monroe (1990) recognized39 speciesin 6 Carretera antigua a CoatepecKm 2.5, Apartado genera.The Africantrogons in the genusApa- Postal 63, Xalapa, Veracruz 91000, . E-mail: 1oderma(three species)are endemicto moun- [email protected] tain forestsin Liberia, Nigeria, Cameroon,An-

937 938 ESPINOSADE LOS MONTEROS [Auk, Vol. 115 gola,Zaire, Uganda,Kenya, Tanzania, Mozam- Heterotrogon;Ridgway (1911) divided the bique,and Malawi. The secondlargest genus, Trogoninto four different genera(Trogon, Cu- Harpactes,contains 11 speciesthat occur in rucujus,Trogonurus, and Chrysotrogon);and Pe- southeastern Asia from India and Sri Lanka to ters (1945) split Priotelusinto two genera(Pri- southeasternChina, and southalong the Malay otelusand Temnotrogon)and the Africantrogons Peninsulathrough Sumatra, Borneo, Java, and into two genera (Apalodermaand Heterotrogon). the Philippines.The monotypic genus Euptilotis I used mitochondrialcytochrome-b (cyt-b) is endemic to mountain forests of western Mex- and 12Sribosomal RNA (12S) genesequences ico and southernArizona. The five speciesof to studyphylogenetic patterns in the Trogoni- the genusPharomachrus are distributedfrom formes. Variation in nucleotide substitution southern Mexico to , Bolivia, Colombia, rates in DNA sequenceshas been correlated Venezuela, Ecuador, and Amazonian Brazil. with codonposition, gene region, and substi- Priotelusincludes two speciesendemic to the tution type. Thus, phylogeneticrelationships Caribbeanislands of and . Fi- amongrecently divergent taxa can be studied nally,the largestgenus in the order,Trogon (17 using rapidly evolvingthird-codon positions, species),is distributedfrom southwesternNew as well as transitionsubstitutions in general. Mexico and southeastern Arizona south For taxa that have diverged long ago, more throughMexico and CentralAmerica to north- slowly evolving transversionsor non-silent ern Argentina. substitutionscan be used.The cyt-b genehas Althoughthe natural history of sometrogons beenshown to containphylogenetic signal at is well known (e.g. Skutch1942, 1944, 1948), severaldifferent phylogenetic levels (Edwards their phylogeneticrelationships remain poorly et al. 1991, Smith and Patton 1991, Moritz et al. understood.Systematic studies have been re- 1992).Some investigators have concludedthat stricted mainly to descriptionsof the informationcontained in cytb is inadequate (e.g. Clark 1918, Zimmer 1948, Clancey1959, to resolveall phylogeneticproblems (Graybeal Parkes1970). Moreover, technical diagnoses of 1993,Avise et al. 1994),and othershave sug- the differentgenera do not clearlydefine the gestedthat analysesbased on individualgenes boundariesof thesetaxa; instead,genera and havea low probabilityof recoveringentire ge- subgeneraare diagnosedprimarily usingpoor- nome trees. Cummingset al. (1995) proposed ly defined morphologicalcharacters that fre- that at least 8,000 contiguousnucleotide sites quentlyunite conflictinggroups or are so am- would be requiredto reacha 95% probability biguous as to be uselessfor inferring mono- of obtainingthe entiregenome phylogeny. As phyly. Characterssuch as the amountof feath- a consequenceof theseconsiderations, the mi- ering on the tarsi, serrationof the tomium, tochondrial 12S gene was included in this presenceof patchesof bareskin, color patterns, study to complementthe cyt-bdata. The 12S and some skeletal features have been used to genehas a slowerevolutionary rate than cyt b, infer relationshipsamong trogons (Ogilvie- making it suitablefor resolvingdeep diver- Grant 1892,Ridgway 1911,Clark 1918,Parkes gences(Hay et al. 1995, Heise et al. 1995). 1970).Many of thesecharacters show a greater range of variation within taxa than among METHODS them,thus leading to someconflicting conclu- Taxaexamined.--Sequences of the cyt-band the 12S sions.Some early classificationslumped most geneswere determinedfor 20 speciesof trogons.Se- of the speciesin the genusTrogon and placed quenceswere deposited in GenBank and are avail- the few remaining speciesin Pharomachrusable through the followingaccession numbers (cyt b (Gould 1875). On the other hand, the use of the and 12S, respectively): (Apaloderma characters listed above has led other ornithol- narina [U94798, U94812]), Bar-tailed Trogon (A. vit- ogiststo proposemultiple subdivisionswithin tatum [U89200, U89234]), Crested (Pharo- the Trogoniformes.Swainson (1837), for ex- machrusantisianus [U89204, U89235]), Golden-head- ed Quetzal (P. auriceps[U94799, U94813]), Pavonine ample, recognizedTrogon, Harpactes, Apaloder- Quetzal (P.pavoninus [U94800, U94814]), Eared Tro- ma, Temnurus,and Calurus; Ogilvie-Grant gon (Euptilotisneoxenus [U89203, U89236]), Cuban (1892)split the Asiantrogons into two genera Trogon (Priotelustemnurus [U89202, U89237]), Black- (Harpactesand Hapalarpactes); Sharpe (1900) di- tailed Trogon (Trogonmelanurus [U94805, U94819]), videdthe Africantrogons into Hapaloderma and White-eyedTrogon (T. comptus[U94804, U94818]), October1998] PhylogenyofTrogoniformes 939

White-tailed Trogon (T. viridis [U94803,U94817]), Subfragmentswere amplified using the following (T. mexicanus[U94809, U94823]), conditions: 2 s at 94øC, 0 s at 47øC, and 15 s at 71øC (T. elegans[U94806, U94820]), Col- for 35 cycles at slope 7. All PCR experimentswere lared Trogon (T. collaris[U94808, U94822]), Masked conductedalong with positiveand negativecontrols Trogon (T. personatus[U89201, U89238]), Black- to test for contamination.Aliquots of 3 gL were vi- throatedTrogon (T. rufus [U94807,U94821]), Blue- sualizedas describedabove. The remainderwas pu- crowned Trogon (T. curucui[U94801, U94815]), Vi- rified to eliminate PCR primers, dNTPs, enzyme, olaceous Trogon (T. violaceus[U94802, U94816]), and buffer componentsusing the GeneCleanII kit Diard's Trogon (Harpactesdiardii [U94797, U94811]), (BIO 101,Inc.). PurifiedPCR productswere subject- PhilippineTrogon (H. ardens[U94796, U94810]), and ed to cyclesequencing using the ABI PrismDye Ter- Orange-breasted Trogon (H. oreskios [U89199, minatorCycle Sequencing Ready Reaction kit with U89239]).The LesserRoadrunner (Geococcyx velox AmpliTaq DNA PolymeraseFS on the GeneAmp [U89198, U89212]), Hodgson'sHawk-Cuckoo (Cucu- PCR System 9600 (Perkin Elmer). Amplifications lusfugax[U89197, U89210]), Greater Coucal(Centro- were performedin 6-•L reactionvolumes containing pussinensis [U89196, U89211]), SpeckledMousebird 2.5 gL of the Prismkit reagent,1 pmoleof sequenc- ( striatus [U89175, U89218]), White-headed ing primer, 5 ng/gL dsDNA template,and 2 gL of (C. leucocephalus[U89173, U89217]), and ultrapure water. Cycle sequencingwas performed White-backed Mousebird (C. colius [U89174, using the followingconditions: 10 s at 95øC,5 s at U89216])were employedas outgroups for character 50øC,and 3 min at 60øCfor 32 cycles.The excessof polarizationand for rootingthe phylogeny.Tissue Taqdideoxy terminators was removedwith Centri- sampleswere obtainedfrom: GeneticResources Col- Sep spin columns (PrincetonSeparations) in a vari- lection,Academy of Natural Sciencesof Philadel- able speedmicrocentrifuge at 2,500 rpm for 2 min. phia; Institute of Zoology,University of Copenha- Final purificationswere dried in a vacuum centri- gen;Department of Ornithology,American Museum fugeand resuspended in 2.5 gL of theloading buffer of Natural History; Museumof Natural Science,Lou- (6x deionizedformamide, 1 x 50 mM EDTA pH 8.0). isianaState University; Collection,University of Resuspendedsequencing products were subjected to Arizona; Museo de Zoolog•a,Facultad de Ciencias, 4% polyacrylamidedenaturing gel electrophoresis in Universidad Nacional Aut6noma de M•xico; and the ABI Prism 377 DNA Sequencer(Perkin Elmer). ZoologicalReference Collection, National University Sequencefiles were analyzed with the aid of the pro- of Singapore. gramSequencher version 3.0 (GeneCodes Corpora- DNA extractionand sequencing.--Totalgenomic tion). A large degreeof fragmentoverlap, as well as DNA was extractedfrom frozentissue using a Chel- sequencingboth DNA strands, ensured accurate ex 5% solutionfollowing the protocolsuggested by data collection.Initial alignmentof the 12Ssequenc- Singer-Samet al. (1989).Target genes were amplified eswas performed using the programMalign (Whee- and isolatedas single fragmentsusing specifically ler and Gladstein1992). Structural regions in the 12S designedPCR primers.This first amplificationwas sequenceswere delimited according to the proposed conductedin Peltier-effectthermocyclers (MJ Re- secondarystructure for the 12S molecule(Springer search)according to the parametersand conditions and Douzery 1996,Houde et al. 1997,Mindell et al. suggestedby Nunn et al. (1996).PCR productswere 1997). subjectedto horizontal electrophoresisin a 2% Phylogeneticanalysis.--All cyt-b nucleotideposi- NuSieve low-melting point agarosegel (FMC Bio- tions and only alignment-stablenucleotides of the products).Gels were stainedfor 10 min in a solution 12S were used in parsimony analysesconducted of 2 pg/mL of ethidium-bromideand visualizedun- with the program PAUP 3.1.1 (Swofford 1993).Be- der UV light. The double-strandedDNA (dsDNA) causeof the large numberof taxa used,it was nec- productswere cut directly from the gel and resus- essaryto usea heuristicalgorithm for searchingthe pendedin 150 gL of ultrapure water by heatingto tree .Input order bias was minimized by per- 73øCfor 15 min. The geneswere reamplifiedas su- forming 1,000replicate heuristic searches with ran- bfragmentsof about 400 bp using internal oligonu- dom additionof taxa.During all analyses,nucleotide cleotideprimers. LPhe (L1243)5'-CAAACAAAGCA- transformations were considered unordered. Char- TGGCACTGAAG-3' and 12Sd (H1883) 5'-TTCGAT- acter stateswere optimized using delayedtransfor- TATAGAACAGGCTCCTC-3'primers were designed mation (DELTRAN), which favorscontemporaneous by J. Groth (unpubl.data; numberedfollowing the changes(i.e. parallelismsover reversals).Branch chickenmitochondrial genome [Desjardins and Mo- swappingwas madeby the tree bisection-reconnec- rais 1990]). The remaining primers used are de- tion algorithm. Retention and consistencyindices scribed elsewhere(Helm-Bychowski and Cracraft werecomputed to evaluatethe levelof homoplasyin 1993,Knight and Mindell 1993).An air thermocycler the most-parsimonioustree. Finally,tree robustness (IdahoTechnologies) was used to perform40-gL am- was examinedusing 500 bootstrapreplications (Fel- plificationsof thesesubfragments in glassmicrocap- senstein1985, Hillis and Bull 1993)and branchsup- illary tubes using standard buffers (Wittwer 1992). port (Bremer1988, 1994). 940 ESPINOSADE LOS MONTEROS [Auk, Vol. 115

Genetic distanceand partition-homogeneitytest.--I (18.2%)between T. elegansand A. narina(Table calculatedcorrected pairwise distancesfor the nu- 1). The smallest distance between different cleotidesequences to test for saturationeffects (Arc- genera was 144 nucleotide substitutions tander 1991, Maynard-Smith and Smith 1996). Dis- (12.6%) between E. neoxenusand P. pavoninus. tanceswere computedwith the program DNADIST from the Phylip 3.5p package(Felsenstein 1993) us- Similar patterns were observedwhen only ing Kimura's two-parametermodel (Kimura 1980) transversion substitutions were analyzed. and assuming a 10:1 transition-transversionbias. Transversiondistances in cyt b rangedfrom six This bias is considered a conservative estimate for (0.5%) between T. curucui and T. violaceusto 78 birds (Kocher et al. 1989, Nunn and Cracraft 1996, (6.8%) between H. oreskiosand T. mexicanus. Espinosade los Monterosand Cracraft1997). Transversiondifferences within Trogondif- Using simulation analysis, Bull et al. (1993) fered by an order of magnitude(six [0.5%]be- showed that phylogeniesare less accuratewhen tween T. violaceusand T. curucuito 52 [4.6%] be- combining DNA partitions having different evolu- tween T. viridis and T. mexicanus). tionary rates comparedwith analysisof data sets Multiple insertionsand deletionscharacter- consistingonly of slowly evolving partitions of the genome.Following this suggestion,I conducteda ized the hypervariableregions within the 12S partition-homogeneitytest. This analysiswas per- gene.Although the multiple alignmentfor the formedwith the aid of the program PAUP*(Swofford 26 taxa sequencedhad a length of 1,016 posi- 1995). One thousandreplicates were generated,and tions, the number of nucleotidesranged from the sumof treelengths was estimated using heuristic 949 in P. temnurus to 975 in A. narina. Functional searches. regions(i.e. stemsand loops)in the sequences were easilyidentified following the modelpro- RESULTS posed for the secondarystructure of the 12S molecule(Springer and Douzery 1996, Houde Sequencevariability.--The combined sequenc- et al. 1997,Mindell et al. 1997).The alignment es of the cyt-b and 12S genesresulted in an contained590 invariantpositions (58%), 72 au- alignment of 2,159 nucleotides.The cyt-b se- tapomorphies(7%), and 354 phylogenetically quences contained 590 invariant positions informativecharacters (35%). The stemregions (52%),85 autapomorphiccharacters (7%), and of the molecule were more conservative than 468 phylogeneticallyinformative characters the loops.Stems encompassed 315 of the in- (41%). The variabilitywithin the three codon variantcharacters (53%), 20 of the autapomor- positionswas similar to that reportedfor other phies(28%), and 134of the phylogeneticallyin- cyt-b genes(Edwards et al. 1991, Irwin et al. formative characters (30%). Hypervariable 1991, Graybeal 1993). Secondpositions were fragmentsproducing ambiguousalignments the least variable codon sites, with 57 nucleo- were locatedmainly insidethe loops. tide substitutions,followed by first positions Variation in the 12S gene between trogon with 137. Third positionswere the mostvari- speciesranged from 19 (1.9%)between P. auri- able, with 362 nucleotide substitutions. Al- cepsand P.antisianus to 150 (14.8%)between A. though the highest variation was presentin vittatumand two speciesof Trogon(Table 2). third-codon positions, only a few of these The averagedistance between species belong- changesinvolved amino acid replacements. ing to different generawas 130 nucleotidesub- Amongthe translatedsequences, 118 (31%)of stitutions (12.8%). Transversion distances the 380 amino add residues were variable. rangedfrom 1 (0.1%)between T. curucuiand T. Basedon the structural model for cyt b pro- violaceusto 48 (4.7%) between A. vittatum and posedby Howell (1989),the highestincidence T. collaris. of hypervariableamino acid residueswas lo- Variation in the transition-transversion ratio catedinside the transmembraneregions of the due to differencesin selectionpressure within molecule,especially in the fourth, fifth, and mitochondrialDNA producesa characteristic eighth segments.This replacementpattern is nucleotidebias especiallyat silent positions consistentwith that reportedfor cyt b in other (Brown 1985, Sueoka 1988). The nucleotide organisms(Diegli-Espoti et al. 1993). compositionand bias (C) in cyt b reportedfor Empiricalpairwise differencesbetween spe- other birds (Nunn and Cracraft 1996, Nunn et ciesof trogonsin cyt b ranged from 62 (5.4%) al. 1996) and for mammals (Irwin et al. 1991) betweenTrogon violaceus and T. curucuito 208 are almost identical to those observed in this October1998] Phylogenyof Trogoniformes 941 942 ESPINOSADE LOS MONTEROS [Auk, Vol. 115 October1998] Phylogenyof Trogoniformes 943

study (Table3). Becausethird-codon position substitutions tend to be silent, and therefore the mostvariable, a highernucleotide compo- sitionalbias was found (C = 0.414).Third po- sitionsare rich in cytosine(42.4%) and adenine (38.6%),much lower in thymine (15.4%),and lowest in guanine (3.5%). Secondpositions havean intermediate bias (C = 0.22),being rich in thymine (39.7%) and poor in guanine (12.8%),with intermediatepercentages for cy- tosine(26.7%) and adenine(20.8%). First posi- tionsare the leastbiased (C = 0.073),being rel- atively rich in cytosine(28.5%) and poor in guanine (20.8%), but intermediate in adenine and thymine(27% and 23.7%respectively). Of the two structuralregions of the 12S(Ta- ble 3), loopspossessed the highestbias (C = 0.191).The biasis mainlyproduced by an over- abundanceof adenine (39.2%), which is ex- plainedby thehypothesis that the low polarity of adeninemay favorhydrophobic interactions with proteins(Gutell et al. 1985).Following ad- enine are cytosine(25.1%), thymine (20.1%), and guanine (15.6%). A more uniform nucleo- tide biasis observedin stems(C = 0.044),being slightlyrich in cytosine(27%) and poorin ad- enine(23%), with intermediatepercentages for guanine(26.7%) and thymine(23.7%). The nu- cleotidecomposition and bias observedin the 12S sequenceswere consistentwith thosere- portedpreviously for mammals(Springer et al. 1995,Springer and Douzery 1996). Several molecular studies have shown the ex- istence of nuclear pseudogenesformed by translocatedfragments of the mitochondrial genome,especially from cyt b (Quinn 1992, Smithet al. 1992,Kornegay et al. 1993).Five ob- servationsindicate that the sequencesused duringthis study were of mitochondrialorigin only: (1) nonsensecodons for protein-coding genesand frameshifts,which are typicalindi- catorsof nuclearcopies, were not apparent;(2) geneswere isolatedinitially as a single frag- ment includingflanking regions of the tRNA- Thr andthe last90 basesof ND5 for cyt b, and the 3' end of the tRNA-Phe for 12S; isolation of entire genesminimizes the potential risk of amplifyingsmaller fragments that are more likely to be translocatedinto the nuclearge- nome;(3) the 381 amino acid codonsforming the cyt b were translatedusing the mitochondrialcode without ambiguitiesor in- termediate stop codons; (4) the secondary 944 ESPINOSADELOS MONTEROS [Auk,Vol. 115

200 _ - ß 1stpositions . creasedrapidly in relation to correcteddis- tances,but after 13% of differenceit beganto 180- o 2ndpositions •'"' level off into a zone of saturation. A globalparsimony analysis of the two com- 140' '"3rd positi bined sequences,including all substitutional 120 variationregardless of positionand type, re- suitedin three equallyparsimonious trees of 100160 'of 3,760steps in length.The strictconsensus tree 80 " (Fig. 2A) confirmedthat eachgenus within the Trogoniformesis monophyletic,but the rela- tionshipsamong genera were only partially re- 40 •' " ß solved.The 10 speciesin the genusTrogon are equally divided into two subcladesthat form oneof the bestsupported lineages within the phylogeny.In one of the subclades(the "Vio- 0 5 10 15 20 25 30 35 laceoussubclade"), T. curucuiis the sistertaxon to T. violaceus;their closestrelative is T. viridis, FIG.1. Saturationplots for thecytochrome-b gene and at the base of this subclade are T. melanurus sequencesconstructed using empirical differences and its sistertaxon T. comptus.The other sub- for eachcodon position as a functionof correctedse- quencedivergence (%) and using the Kimura two- (the "Elegantsubclade") is composedof parameter model with a 10:1 transitions:transver- T. mexicanus,T. elegans,T. rufus,T. collaris,and sion ratio. T. personatus.Excluding the last two species, whichare each other's closest relative, the phy- logeneticrelationships in this subcladeare un- structurededuced from the 12Ssequences was resolved.The sistergroup of Trogonis Priotelus entirelyconsistent with thatproposed for other (CubanTrogon). The next node of the consen- (Springer and Douzery 1996,Hou- sustree is a polytomyformed by Trogon-Priote- de et al. 1997,Mindell et al. 1997);and (5) the lus, Pharomachrus-Euptilotis,and Harpactes. nucleotidebias observedin the differentgene Within quetzals,Pharomachrus antisianus and P. partitionsis nearlyidentical to thosereported pavoninusare sister species, their sister group is for otherbirds (Moore and DeFilippis 1997). P.auriceps, and the sistertaxon to the quetzals Phylogeneticanalysis.--The homogeneity test is the monotypicEuptilotis neoxenus. In the showedthat the datamatrices for the cyt-b and cladeformed by the Asiantrogons, Harpactes 12S sequencesrepresent homogeneous parti- diardii is the sister to H. ardens,and their tions (P = 0.034). Therefore,a combinedanal- sistergroup is H. oreskios.The two Africantro- ysis approachwas chosenfor phylogenyesti- gons(Apaloderma), the mostbasal species in the mation. In addition, empirical pairwise dis- cladogram,are sistertaxa to the rest of the or- tanceswere plotted againstKimura distances der.Although the consensustree shows an ap- to detectsaturation in thedifferent partitions of parent lack of resolution,the nodesare sup- eachgene. This analysisshows that the nucle- portedwith highbootstrap values at thegenus otide substitution rate follows a linear relation level and above.Relatively low bootstrapval- in the 12S gene. Evidenceof saturationoc- ues were registeredfor the cladecomprising curredonly in thecyt-b gene. Figure 1 presents the Asiantrogons (79%) compared with values comparativecurves for the accumulationof to- for the othergenera. tal substitutionsdepending on codonposition The African trogons, quetzals,and New in the cyt b. Secondpositions showed a clear World Trogonswere eachidentified in 100%of linear patternand had the slowestrate of nu- the bootstrapreplications. In contrastto inter- cleotidesubstitution (best fitted line slope = specific patterns, intergenericrelationships 0.77).The nucleotidereplacement rate in first were poorly supported(<50%). The only ex- positions(slope = 1.81) was more than twice ceptionwas the lineagerelating E. neoxenusto that for secondpositions, but the accumulation the quetzals,which had a bootstrapvalue of maintainedessentially a linearpattern. The nu- 100%.Finally, the monophylyof the Trogoni- cleotidesubstitution rate at third positionsin- formeswas highly supported,scoring boot- October1998] PhylogenyofTrogoniformes 945

lOO% A 100% 99% 95% viridis

Trogonmelanurus melanurus lOO% 100%

-- Trogonmexicanus -- Trogonmexicanus Pr•telus temnurus Priotelus temnurus 79%r•.•pharomachrus antisJanus 75%,•.•pharomachrus antis•anus 100%[ t• pharomachruspavoninus 100ø/[•I.• pharomachruspavoninus • pharotnachrusauriceps 00ø[• I pharomachrusauriceps I ' Euptilotisneoxenus 100% • Euptilotisneoxenus 1 I 100%r•.[•Harpacres diardii 100o?.•• Harpactes diardii [ 79%I I• Harpactesardens 80%I I• Harpactesardens -- Harpactesoreskios • Harpacresoreskios 100%•Apalodernta narina Apalodermanarina • Apalodermavittatum 100%C Apaloderma wttatutn Out•roup Out•roup

100% Trogoncurucui 100% Trogoncurucui C Trogonviolaceus D lOO% Trogonviolaceus -- •Trogonvirb:iis Trogoncomptus Trogoncotnptus 100% Trogonmelanurus 100•/i•Trogonviridis -- Trogonelegans Trogonelegans -- Trogonrufus Trogonrufus Trogoncollaris Trogoncollaris Trogonpersonatus Trogonpersonatus -- Tragonmexicanus 100•/100o/•-- Trogonmelanurusmexicanus 70% pharomachrusantisJanus F 100Yo65% pharomachrus antisJanus pharomachrusauriceps pharomachrusauriceps 100%1• pharomachrusEuptilotis neoxenus pavoninus 100%10&•PharomachrusEuptilotis ne•oxenus pavoninus lOO% Priotelus temnurus Priotelus temnurus 100o/or•_•Harpacres diardii 81% Harpactesardens 100o/•HarpactesHarpacresdiardiioreskios 1 86%I • Harpacresoreskiosardens 100% E Apalodermanarinavittatum 100% [•• Apalodermanarinavittatum Outgroup Outgroup

FIG.2. Phylogenetichypotheses for the Trogoniformes.(A) Strictconsensus tree from three equally par- simonioustrees obtained from equal-weightinganalysis of all nucleotidepositions in both genes(length, 3,760;consistency index, 0.407; retention index, 0.5). (B) Strict consensus tree from two equally parsimonious treesobtained after down-weightingthird-position transitions (0.5:1) for cytochromeb (length,3,157; con- sistencyindex, 0.466; retention index, 0.573). (C) Strictconsensus tree from two equallyparsimonious trees obtainedafter down-weightingthird-position transitions (0.2:1) for cytochromeb (length,2,795; consistency index,0.464; retention index, 0.571). (D) Strictconsensus tree from two equallyparsimonious trees obtained after down-weightingthird-position transitions (0.1:1) for cytochromeb (length,2,673; consistency index, 0.465;retention index, 0.572).Percentages on branchesare bootstrapvalues of 500 replications.For taxa in- cludedin the outgrouprefer to Taxaexamined in Methods. strapvalues of 100%even when the outgroup havebeen hit multipletimes (i.e. 362 of 381).To wasnot constrainedto be monophyletic. filter this saturation effect, I decided to down- Onepossible reason for thelack of resolution weight transitionswith respectto transver- in deepernodes of the tree maybe the homo- sions.In the first analysis,third-position tran- plasydue to multiplehits in third positionsof sitions(cyt b only)were down-weighted to half cyt b. More than 95% of third-codonpositions the value of third-positiontransversions. This 946 ESPINOSADE LOS MONTEROS [Auk, Vol. 115

100% -- Trogoncurucui i 24 98% Trogonviolaceus 9O% Trogonviridis Trogoncomptus 22 Trogonmelanurus 100% -- 23 71% Trogonelegans Trogonrufus Trogoncollaris 3o% Trogonpersonatus Trogonmexicanus

54% I Pharomachrus antisianus 43% 100% -- Pharomachruspavoninus Pharomachrusauriceps 41% Euptilotisneoxenus

Priotelus temnurus

lOO% Harpactesdiardii 81% Harpactesardens Harpactesoreskios Apalodermanarina 00%ß Apalodermavittatum Outgroup

FXG.3. Singlemost-parsimonious tree obtainedfor a combinedanalysis of both genesafter removing third positionsfrom the cytochrome-bsequences (length, 1,971; consistency index, 0.466;retention index, 0.574).Percentages are the valuesof 500 bootstrapreplications; numbers in front of the nodesare branch support values. resultedin two equally parsimonioustrees of Worldtrogons (Fig. 2D). Althoughin this anal- 3,157steps. The consensus tree (Fig. 2B) did not ysis,the polytomyin the "Elegantsubclade" supportmonophyly of the New Worldgenera. within Trogonwas resolved,the relationships In this tree, quetzalsare placed as a sister amongthe NewWorld genera were ambiguous. groupof the Asian trogons,a relationshipnot Based on the above results, I excluded third- supportedin thebootstrap test. Once third-po- positioncyt b from the data matrix and per- sitiontransitions were down-weightedto a ra- formed a new parsimonyanalysis, which re- tio of 0.2:1 with respectto transversions,the sulted in a single most-parsimonioustree of New World genera formed a monophyletic 1,971steps in length(Fig. 3). In this phyloge- clade(Fig. 2C). The interrelationshipsamong netichypothesis, all the generawere resolved the New World,Asian, and Africantrogons, as monophyleticand supportedby highboot- however, were unresolved. Further down- strap values(>80%) as well asbranch support weightingthird-position transitions (from 0.1 (>6). The New Worldgenera were monophy- to 0.025 transitions per transversion)consis- letic, and their sister taxon was Harpactes tently produced two alternative trees of 2,673 (Asiantrogons). The most basal group was the steps.The consensusof thesetrees placed the African genus Apaloderma.Within the New Africantrogons as the mostbasal lineage, and World lineage,the two subcladesof Trogon the Asian trogonsas the sistertaxa to the New were recoveredand the interspeciesrelation- October1998] Phylogenyof Trogoniformes 947 shipswere congruentwith thoseobtained in vicariancebiogeography assumes that the an- the previous analyses(Fig. 2D). The sister cestral area must be considered as the sum of groupto Trogonwas the lineageformed by Eup- all the areasin which the groupis found.How- tilotis-Pharornachrus.Finally, Priotelusternnurus ever,this implies that the distributionof the an- was the sister taxon to the rest of the New cestorwas morewidespread than that of any of Worldgenera. This phylogenetic hypothesis re- its descendants(Bremer 1992). Recently, Bre- mained constant even when the taxa included mer (1992, 1995) proposeda method for esti- in the outgroupwere changed.By removing mating the relative probability that different the saturatedpartition within cyt b, a consid- areas were part of the ancestralarea of the erable amount of noise was eliminated, reduc- group. This relative probability is computed ing the length of the tree by 1,789 steps(i.e. based on a gain-lossratio of individual areas from 3,760 stepsequal weightsto all nucleo- after being coded as binary characterson a tides, to 1,971steps without the 381 third-co- cladogramassuming irreversibility. don positions).In spiteof thenoise elimination, ApplyingBremer's method to the cladogram however,the supportvalues for the nodeslink- proposedhere (Fig. 3), Africa has a probability ing different genera did not improve signifi- of 1.0 becauseit has been gained onceon the cantly.The nodeslinking the New World gen- Apalodermalineage and then lost once on the era to Priotelusand then to Harpacteswere lost clade encompassingthe remaining genera. in trees one step longer than the most-parsi- monious solution. Asia and the New World eachreceive a prob- ability of 0.5. Asia is gainedon the lineagelead- ing to Harpactes,then is lostonce in Apaloderma, DISCUSSION and once in the New World clade. In the same manner,the New World is gained oncein the On the origin and distributionof Trogonifor- clade formed by the Neotropicalgenera and tues.--Fromthe standpointof biogeography, then lost oncein Apalodermaand oncein Har- the trogonshave been an enigmabecause of pactes.Therefore, the idea of a Neotropicalori- their Pantropical distribution (Darlington gin is not supported.Instead, an African origin 1957).Their currentdistribution coincides with for trogons seems a reasonable conclusion, the distribution of several other avian families with the New World representinga secondary (e.g. Anhingidae,Capitonidae, Heliornithidae, center of radiation. Ronquist's(1994, 1995) Jacanidae,Psittacidae) and other vertebrates method,as well as Brundin's(1981, 1988)pro- (e.g. crocodilians and caecilians).Congruent gressionrule, identify Africa as being the an- biogeographicpatterns between or amongtaxa cestralarea of the Trogoniformes. can be explainedby two processes:speciation Additional evidence supporting an Old of widespreadtaxa after a vicariant event, or World origin for trogons comesfrom paleon- multiple dispersalevents. Although vicariance requiresthe fewestad hoc assumptionsto jus- tology.The oldestdescribed within the tify distributionpatterns, it dependson phy- Trogonidaehave been found in Tertiary logeneticcongruence using corroboratedphy- depositsof (Olson 1985). The earliest logeniesfor othertaxa. These are currentlyun- comes from the middle Oligocene of available. Switzerland and has been referred to Protornis Reconstruction of ancestral distribution ar- glarniensis.This speciesclearly showsthe het- eas can be addressedfor trogons.Early hy- erodactylcondition typical of the Trogonidae pothesespointed to the New World as the cen- (Olson1976). Another fossil species, Paratrogon ter of origin for these birds (Swainson1837, gallicus,was recoveredfrom lower Miocenede- Ridgway 1911). This idea was based on the positsat Langy,France (Olson 1976). Currently, high diversity of trogons in the Neotropics Gerald Mayr (pers.comm.) is describinga new (64% of species).Cain (1971),however, argued fossil trogon from the Middle Oligocene(33 that the areain whichmost species of a partic- million ago) of C•reste, France.In con- ular group are distributed may be a secondary trast, the oldest fossils discovered in the New center of diversification. Therefore, relative World belongto two extant species(Priotelus ro- speciesrichness may be false evidencefor in- seigasterand Trogonsurrucura), which are ferringthe ancestralarea of a taxon.Traditional known from Pleistocenedeposits from the Do- 948 ESPINOSADE LOSMONTEROS [Auk, Vol. 115 minican Republic and Brazil, respectively approximatetimes can be estimatedbased on (Brodkorb 1971). differences in nucleotide substitutions in mi- Consideringthat Africa is one of the largest tochondrialDNA (Brownet al. 1982,DeSalle et continents,how can one explainthat only 8% al. 1987,Miyamoto and Boyle1989, Irwin et al. of the extantspecies of trogonsare distributed 1991).The existenceof a molecularclock has there?In general,the overallbiological diver- beenquestioned because of evidenceshowing sity of Africa is relativelylow comparedwith that differentregions of the genomeevolve at othertropical areas (Keast 1973). Identifying all different rates in different lineages(Martin et of the possibleelements that determinediver- al. 1992, Martin and Palumbi 1993). Most of sitypatterns though and space is extreme- theseexamples involve lineages whose species ly difficult.Many differentphysical, historical, exhibit significant differencesin body size, and biologicalfactors have been correlated metabolicrate, or generationtime. Trogons,by with almostevery patternof variationin spe- contrast,are ratheruniform in body size and ciesdiversity (Huston 1994). The principleof generation time. competitiveexclusion (Hardin 1960)might be Characteristicsobserved in the sequencesof one of the factors that could be invoked for the the cyt-bgene of trogons(Tables 1-3) are sim- smaller number of speciesof trogonsin Africa ilar to thoseobserved in albatrosses(order Pro- andAsia versus the Neotropics. The Old World cellariiformes),in which correctedthird-posi- speciesof trogonsare insectivorous,whereas tion divergencewas estimated at a rate of 1.58% the New World speciesfeed on a mixture of and 2.86% for per million years (Nunn et al. fruits and .Possibly, the fruit-eating 1996). Using these estimates,and assuming nichesin the Old Worldare taken by avianfam- that the correctedthird-position divergence ilies that are poorlyrepresented or completely amongthe trogonsis linear with respectto missingin the New World (e.g. Bucerotidae, time, a rough date for the separationtimes Musophagidae,Irenidae, Pycnonotidae). Con- among generacan be suggested.The genera sequently,a decreasein competition pressure Pharomachrusand Euptilotisdiverged 13.8 to 25 may have resultedin radiationtoward new niches in the New World. million yearsago (Mya). If we comparethese dates with others estimated for corvine birds Other factors that have been associated with (Helm-Bychowskiand Cracraft1993), the tro- speciesdiversity are structural and climatic heterogeneityof the habitat (Schluter1988, gons represent a relatively old divergence Huston1994). During phasesof glacialaridity, within birds. A mean value of 51.5%for pair- the rain forest in the Amazon and Southeast wise correctedthird positiondivergence gives Asia shrankto isolatedrefugia (Roberts 1984), estimatesof the dateof originfor the Neotrop- possiblyconstituting favorable conditions for icaltrogons between 18 and32.6 Mya. The split the speciationof the populationsrestricted in of the Africantrogons with the restof the gen- these areas. Compared with SoutheastAsia era occurred between 19.7 to 35.6 Mya. Even and the New World,the tectonichistory of Af- with suchbroad estimates, these data suggest rica wasrelatively stable during the last40 mil- that the radiationof the major cladesof tro- lion yearswithout being affected by the riseof gons,especially among Africa, Asia, and the extensivemountain ranges (Potts and Behrens- New Worldmay be characterizedas a starphy- meyer1992). Thus, a high diversityin South- logeny.If the major cladesdiversified rapidly, eastAsia and especiallyin the New Worldmay that might be responsiblefor the problemsin be a direct consequenceof the great orogenic recoveringa stablesignal during cladisticanal- activityduring the late Cenozoic due to thecol- ysis.Finally, trogons diverged from their sister lision of continentalplates, and not the result taxon (i.e. Coliiformes) between 25.5 to 46.1 of a longhistory of theavifauna within suchar- Mya. This estimateis consistentwith the date eas. suggestedby the oldest fossilsdescribed for Absolutedates of diversificationfor trogons trogons (Olson 1976, 1985). An undescribed are unknownowing to the lack of an extensive fossil heterodactylbird recoveredfrom the fossilrecord. Nonetheless, the problemof dat- Lower (53 Mya) LondonClay of Essex ing can be approachedthrough molecular (G. Mayr pers.comm.), however, indicates that studies.Several authors have suggestedthat the Trogoniformesorigin should be earlier October1998] Phylogenyof Trogoniformes 949

A B C DE F G

[] [] [] [] [] [] [] Trogoncurucui [] [] [] [] [] [] [] Trogonviolaceus [] [] [] [] [] [] [] Trogonviridis [] [] [] [] [] [] [] Trogoncomptus [] [] [] [] [] [] [] Trogonmelanurus [] [] [] [] [] [] [] Trogonelegans [] [] [] [] [] [] [] Trogonrufus [] [] [] [] [] [] [] Trogoncollaris [] [] [] [] [] [] [] Trogonpersonatus [] [] [] [] [] [] [] Trogonmexicanus [] [] [] [] [] [] [] PharomachrusantisJanus [] [] [] [] [] [] [] Pharomachruspavoninus [] [] [] [] [] [] [] Pharomachrusauriceps [] [] [] [] [] [] [] Euptilotisneoxenus [] [] [] [] [] [] [] Priotelustemnurus [] [] [] [] [] [] [] Harpactesdiardii [] [] [] [] [] [] [] Harpactesardens [] [] [] [] [] [] [] Harpactesoreskios [] [] [] [] [] [] [] Apalodermanarina [] [] [] [] [] [] [] Apalodermavittatum Ou•group

FiG.4. Evolutionarytendencies in the colorationpattern of trogonfeathers. (A) Whitepectoral line di- vidingthe chest and belly color: absent (white); present (black). (B) Color of thebelly: red (white); yellow (black).(C) Colorationpattern on tail :one white spot at thetip of thefeather (white); multiple white bands(hatched); no white pattern (black). (D) Whitespots on the secondary feathers: present (white); absent (black).(E) Color of the back:green (white); brown (black).(F) Color of the head:same color as the back (white);gray (hatched); violet (black), and (G) Colorof the rump:same color as the back(white); violet (black). thanthe datesuggested by thepresent calibra- havea strongsexual component, the following tion. discussionis basedmainly on maleplumages. Colorationpatterns.--Without question, one of For mostspecies, the ventralcoloration pat- the mostattractive features of trogonsis their tern can be divided into two regions:(1) the .Indeed, the Quetzal was chin,throat, and upper portion of the breast considereda sacredbird in many pre-Colum- (whichusually show the samecolor as the head bian cultures of the New World because of its or the back);and (2) the lowerportion of the coloration.The brightest colors and more com- breastand the belly,which typically are red or plex coloration patterns occur mainly on yellow.These two regionsare divided by a regionsof the body that are involvedduring white bandin somespecies. This white band display(i.e. head, upper back, breast, tail, and hasevolved independently at leastthree times surfaceof the wings).Less-exposed areas like withinthe order,once in theAsian trogons (H. theunderparts of thebody usually present dull diardii)and twice in the genusTrogon. This colorsand in most caseslack specialpatterns. whiteband represents a synapomorphy for the A corroboratedphylogeny reveals evolutionary Elegantsubclade (Fig. 4A). "Red belly" canbe tendenciesin thecoloration pattern of trogons. interpretedas ancestralwithin the group,and Becausecolor and color patternsin trogons the derivedcondition "yellow belly" evolved 950 ESPINOSADE LOS MONTEROS [Auk, Vol. 115 oncein the Asian trogons(H. oreskios)and in- of structural complexityin these granules. dependently(twice) in Trogon(Fig. 4B). Quetzalshave the most complexkind of iri- White bandson the tail arecomplex because descence,with barbulespossessing from five patternsdepend on sexand age.Nevertheless, to eight layersof elliptical plateletsforming a the presenceof this charactercan be interpret- continuous mosaic on the iridescent surface of ed as the primitive condition, apparently the Theseplatelets are made of mela- evolvingin two contrastingdirections. It has nin filled with air capsulesdivided by exten- transformedeither from a singleband located sionsof the plateletwall. The layersof plate- at the tip of the featherto multiplebands, or lets are separatedby layers of keratin. In Tro- from oneband to no bands(Fig. 4C). gon,the melanin granulesare air-filled rods Multiple white spotson the secondaryfeath- that are packedso tightly that practicallyno ers,which are more evident in males,vary from keratinseparates them. Trogonsare lessbril- a randomdistribution of tiny dotsto clearlyde- liant than quetzalsbecause the rod arrange- finedwhite bands. The presence of anyof these ment only allowslight to passat an angle of patternsis the plesiomorphiccondition for tro- 30ø, therebyproducing a relatively weak iri- gons,whereas the apomorphicstate is the loss descenteffect (Durrer and Villiger 1966).The of white pattern(i.e. secondariesplain black). differencein colorintensity between the spe- This derived conditionhas appearedindepen- ciesof trogonsis duemainly to changesin the dently twice,once in T. viridisand oncein the diameter of the rods. Thick rods produce Pharomachrus-Euptilotisclade, in whichthe loss goldenglows, whereas thin rodstend to pro- of white patternrepresents a synapomorphy duceblue tones.The othertwo structuralpat- (Fig. 4D). ternsin the iridescentgranules are variations Colorationof the dorsalregion can be divid- fromthat describedfor Trogon.In Priotelus,the ed into threegeneral areas: (1) the head,(2) the total diameter of the rod is similar to that in back, and (3) the rump. Brown back color in Trogon(0.2 ix),but the melanin wall is thicker malesis a synapomorphyfor the Asian tro- in Priotelusthan in Trogon(0.08 IXand 0.04 IX, gons.Thus, the presenceof a greenback is ple- respectively). Another difference between siomorphic(Fig. 4E).The colorof the othertwo thesegenera is that in Priotelus,the melanin dorsal regions(head and rump) is correlated rods are clearly divided by keratin layers.Fi- with the backcolor The plesiomorphicstate for nally, in Harpactesand Apaloderma,the diam- thesetwo regionsis brown in theAsian trogons eter of the rodsis largerthan in Priotelus,and and greenin the African and New World tro- the keratinlayers dividing the rods are more gons.Head colorpresents at leasttwo derived than twice as thick as in Priotelus(Durrer and states,gray and violet. Violet heads evolved Villiger 1966). twice in the New World genera(Priotelus tem- Accordingto the phylogenyobtained in the nurus,and in three speciesof the Violaceous presentstudy, the least-iridescentstructures subclade),whereas gray headsevolved at least occurin African and Asiantrogons, which are oncewithin the Asiantrogons (Fig. 4F). the most basal lineages(Fig. 5). Theselarge Finally,for mostof the speciesI examined the rods divided by thick layersof keratinare rel- rump was the samecolor as the back,the only atively similar to the iridescent structures exceptionwas for three species:Trogon melan- found in other birds (Dorst 1951;Durrer and urus,T. comptus, and T. viridis have violet rumps Villiger1962, 1966). In derivedlineages, rod di- that representthe only derivedcondition ob- ameter and thickness of the melanin wall are servedfor this character(Fig. 4G). reduced. Concomitant with this are a reduction Evolutionof iridescentstructures in trogon in the thicknessof the keratinlayer, an incre- feathers.--Plumageiridescence is widespread ment in the numberof rods,and a displace- in birds. In most bird groupslike humming- ment of the rods toward the external surface of birds and sunbirds,the interferencegranules the barbules.The more complexstructures responsiblefor the productionof iridescent found in quetzalscan be explainedas a step colors are relatively uniform in design and further in the tendencytoward an increased composition acrossspecies (Dorst 1951, Dur- number of rods on the surface of the barbules, rer and Villiger 1962). In trogons,Durrer and finally leadingto the fusion of multiple air- Villiger (1966) describedfour different levels filled rodsinto ellipticalplatelets. October1998] PhylogenyofTrogoniformes 951

Pharomachrus contributingtheft scientificrigor and invaluablecrit- icisms.I gratefullyacknowledge J. Groth for provid- ing 12Sprimers and valuableadvice during the lab- oratory work and G. Mayr for unpublishedinfor- mationon fossiltrogons. i am very thankful to the following individuals and institutionsfor supplying tissue samples:D. Agro (GeneticResources Collec- tion, Departmentof Ornithology,Academy of Nat- ural Sciencesof Philadelphia),P. Arctander (Institute of Zoology,Department of PopulationBiology, Uni- Trogon versity of Copenhagen),G. Barrowcloughand E Sweet (Department of Ornithology, American Mu- seumof NaturalHistory), M. Hafnerand E Sheldon (Museum of Natural Science,Louisiana State Uni- Priotelus versity),T. HueIsand S.Russell (Department of Ecol- ogy and EvolutionaryBiology, University of Arizo- na), A. Navarro-Sigenza(Museo de Zoologia Facul- tad de Ciencias, Universidad Nacional Autonoma de Mexico),and the ZoologicalReference Collection at NationalUniversity of Singapore.Support was pro- vided by grantsfrom the Frank M. ChapmanFund and SanfordFund of the Departmentof Ornithology of the AmericanMuseum of Natural History,and the Graduate Studies Committee of the Ecology and OutgroupApaloderma EvolutionaryBiology Program of the City College, FIG.5. Most-parsimoniousscenario for the evo- City Universityof New York.This researchis a con- lution of iridescent structures in the feathers of tro- tribution from the Lewis B. and Dorothy Cullman gons. microscope photographs were ResearchFacility at the AmericanMuseum of Natu- scannedfrom Durrer and Villiger (1966). Photo- ral Historyand hasreceived generous support from graphswere taken using a 30,000:1magnification the LewisB. and DorothyCullman Programfor Mo- scale. lecularSystematics Studies, a joint initiativeof The New York Botanical Garden and The American Mu- seumof Natural History. I also receivedsupported A phylogeneticclassification of thegenera of Tro- by a Ph.D. grant from the Mexican government goniformes.--Usefulclassifications should be (CONACyT#80276) and by a Frank M. Chapman basedon a corroboratedphylogeny, and the Fund GraduateStudent Fellowship. classification must reflect the historical rela- tionshipsof the taxaencompassed within that LITERATURE CITED group.Based on my tree (Fig. 3), I recommend the following phylogeneticclassification for ARCTANDER,P. 1991.Avian systematicsby sequence generawithin the Trogoniformes: analysisof mtDNA. Pages619-628 in Acta XX CongressusInternationalis Ornithologici (B. D. ORDERTrogoniformes Bell Ed.). Christchurch, New Zealand, 1990. FAMILYTrogonidae New Zealand Ornithological CongressTrust SubfamilyApaloderminae Board, Wellington. GENUSApaloderma AVISE, J. C., W. S. NELSON, AND C. G. SIBLE¾.1994. SubfamilyTrogoninae Why one-kilobasesequences from mitochondri- Tribe Harpactini al DNA fail to solvethe phylogenetic GENUSHarpactes enigma.Molecular Phylogenetics and Tribe Trogonini 3:175-184. GENUS Priotelus BREMER,K. 1988.The limits of amino acid sequence GENUSTrogon datain angiospermphylogenetic reconstruction. GENUS Pharomachrus Evolution 42:795-803. BREIVIER,K. 1992. Ancestral areas: A cladistic rein-

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