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Phylogenetic Relationships Among the Trogons

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Phylogenetic Relationships Among the Trogons The Auk 115(4):937-954, 1998 PHYLOGENETIC RELATIONSHIPS AMONG THE TROGONS ALEJANDRO ESPINOSA DE LOS MONTEROS• Departmentof Ornithology,American Museum of NaturalHistory, Central Park West at 79 Street, New York, New York 10024, USA ABSTRACT.--Theorder Trogoniformescurrently is divided into six genera:Apaloderma, Pharomachrus,Euptilotis, Priotelus, Trogon, and Harpactes.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 Quetzals(Pharomachrus spp.). The most basalgenus within the New World cladewas Priotelus.These results suggest an Old World (Africa/Eurasia)origin 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(order Trogon- Morphologicalfeatures said to be character- iformes)are amongthe mostcolorful of birds. 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 species 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 basal 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, Mexico. 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 genus 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 Peru, 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 Cuba and Hispaniola. 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 subspecies 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):Narina Trogon (Apaloderma characters listed above has led other ornithol- narina [U94798, U94812]), Bar-tailed Trogon (A. vit- ogiststo proposemultiple subdivisionswithin tatum [U89200, U89234]), Crested Quetzal (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 Mountain Trogon (T. mexicanus[U94809, U94823]), conditions: 2 s at 94øC, 0 s at 47øC, and 15 s at 71øC Elegant Trogon (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,
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