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Molecular Phylogenetics of the Genus Piranga: Implications for Biogeography and the Evolution of Morphology and Behavior

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Molecular Phylogenetics of the Genus Piranga: Implications for Biogeography and the Evolution of Morphology and Behavior The Auk 115(3):621-634, 1998 MOLECULAR PHYLOGENETICS OF THE GENUS PIRANGA: IMPLICATIONS FOR BIOGEOGRAPHY AND THE EVOLUTION OF MORPHOLOGY AND BEHAVIOR KEVIN J. BURNS• Museumof VertebrateZoology and Department of IntegrativeBiology, University of California, Berkeley,California 94720, USA ABSTRACT.--Speciesin the genusPiranga vary in degreeof sexualdimorphism, plumage coloration,morphology, song, migratory patterns, and geographicdistribution. To study theseaspects of Pirangabiology in an evolutionarycontext, I constructeda phylogeny for thisgenus using cytochrome-b sequence data. Parsimony and maximum-likelihood analyses of DNA datareveal three possible phylogenies for speciesin thisgenus. All threetrees iden- tify a cladecontaining P. rubriceps, P.leucoptera, and P. erythrocephala and a cladecontaining P.rubra, P. ludoviciana, P.olivacea, P. bidentata,and P.fiava. The trees differ in theplacement of P.roseogularis. Morphology, song, and plumage data did not agreewith thesephylogenies. Levelsof sequencedivergence and the phylogeny of haplotypesare consistent with theidea thatP. fiava as currently described contains more than one evolutionary unit. Mapping the evolutionof seasonalmigration onto the DNA treesindicates that migrationevolved once within Piranga.Received 15 November1996, accepted 20 November1997. STUDYING PATTERNS OF CHARACTER VARIA- plumage.One exceptionto this marked sexual TIONin conjunctionwith a phylogenyprovides dichromatismis P. rubriceps,in which males a powerful methodfor understandinghow and femalesdiffer only in the extentof red col- charactersevolve and for uncovering evolution- orationon the upper breast. ary associationsamong traits (Brooks and Brush(1967) and Hudon (1990)characterized McLennan1991, Harvey and Pagel1991). The the chemicalbasis underlying some of the dra- tanager genusPiranga (Passeriformes: Thrau- maticplumage color in four speciesof Piranga. pidae) providesan excellentmodel for study- In threeof thesespecies (rubra, fiava, and oIiva- ing the evolutionof differenttypes of charac- cea),several common carotenoids were respon- ters.Species in thisgenus vary in the degreeof siblefor red plumage(Hudon 1990). Piranga Iu- sexualdimorphism, plumage coloration, mor- dovicianawas unique among the four speciesin phology,song, migratory patterns, and geo- that the only red pigmentfound was rhodox- graphicdistribution. None of theseaspects of anthin,a dietary-basedcarotenoid. The relative Pirangabiology has been examined in a histor- significanceof thesefindings and patternsof ical, evolutionarycontext because of the lackof plumage-colorevolution need to be addressed a rigorousphylogeny for the group. in a phylogeneticcontext. Although plumage The nine speciesof Pirangahave been placed colorand patternoften are usedto definegen- in this genusand arrangedin a linearclassifi- era and to determinespecies status, their rele- cation(Storer 1970) based on plumagecharac- vanceas phylogeneticcharacters has not been teristics,a stoutlyshaped bill, geographicdis- thoroughlyinvestigated. tribution, and the presenceof sexual dimor- Body size and shape vary considerably phism.One of themore striking features of this among speciesof Piranga.Two species,P. Ieu- genusis theconspicuous plumage coloration of copteraand P.erythrocephaIa, average 33% small- males.Males typically are more colorful than er than the otherseven species. These smaller- females,and males of all specieshave at least sized Pirangawere consideredby Howell and somered plumage.Females are morecryptic, Webb(1995) to belongto a separategenus, Sper- with mainly brown, yellow,or olive-colored magra(Swainson 1827). In addition, somespe- ciesof Piranga(Ieucoptera, erythrocephaIa, and ro- • Presentaddress: Department of Biology,San Di- seoguIaris)have shorter and less-pointed wings ego State University, San Diego, California 92182, than the otherspecies in the genus(Ridgway USA. E-mail: kburns@sunstroke. sdsu.edu 1902).Whether there is a phylogeneticcompo- 621 622 KEVINJ. BURNS [Auk, Vol. 115 nent to this variation cannot be addressed group.Although no singlecharacter defines the without a phylogenyfor this group. genus,two molecularstudies confirm that Pi- Shy (1983,1984a, b, c) detailedintraspecific rangais monophyleticwith respectto othertan- and interspecificsong variation in P.olivacea, P. agers. A study of allozyme variation (Mc- ludoviciana,P.rubra, and P.fiava. In a comparison Donald 1988) showedthat three morphologi- of songcharacteristics of the four species,Shy cally similar species(rubra, olivacea, and ludovici- (1984c)provided data on nine songvariables: ana)form a monophyleticgroup. Furthermore, maximum frequency,minimum frequency,av- a comprehensivecytochrome-b phylogeny of erage maximum frequency,average minimum Thraupidae(Burns 1997) showed that two mor- frequency,average interval between figures, phologicallydistinct species (olivacea and eryth- average duration of figures, frequencyrange, rocephala)form a clade with respectto the 48 averagefrequency range of figures, and num- othertanager genera sampled. Thus, an addi- ber of figuretypes per bird. In conjunctionwith tionalgoal of this studyis to furtherclarify the a phylogeny for Piranga, Shy's information limits of this genus. could addressthe usefulnessof songcharac- teristicsas systematicdata. Vocal information METHODS has provenimportant to systematicquestions at and below the specieslevel, yet few studies Taxonsampling and outgroupchoice.--I used indi- have used songdata to establishrelationships viduals representingall nine speciescurrently as- signedto Piranga(Storer 1970). For all speciesexcept among species(see Payne 1986). P.rubriceps, more than oneindividual was used to re- The geographicdistributions of Pirangaare duce problemsassociated with using only a single centered in Mexico and Central America. Three exemplar per taxon (Table 1). Tanager outgroups species(erythrocephala, bidentata, and roseogular- used included representativesof the generaHabia, is) are endemicto this region,and all but one Chlorothraupis,Calochaetes, and Ramphocelus(Gen- occur there during at least sometime of the Bank Accession numbers AF006213, AF006219, year Pirangafiava and P. leucopteraare wide- AF006233,and U15717 to U15724). Habia and Chlo- spreadin Mexico, Central America, and South rothraupiswere chosenbased on a closerelationship America,and the distributionof P.fiava also ex- to Pirangaidentified by a molecularphylogenetic tendsnorthward to North Americaduring the study of tanagergenera (Burns 1997). I alsoincluded Calochaetesand Ramphocelusbecause the traditional borealsummer Three other species (rubra, lu- linear arrangement of tanagers (e.g. Storer 1970) doviciana,and olivacea)are seasonalmigrants placesthem near Piranga. Multiple sequences of Ram- that spendthe breeding season in NorthAmer- phocelus(from Hackett 1996) were included in order ica and the nonbreedingseason in parts of to increase tree balance and to reduce the branch Mexico, Central America, and South America. lengthleading to this genus(Smith 1994). As an out- The onespecies not foundin Mexicoor Central groupto thesetanager sequences, I used sequence of America during at least part of the year is P. a non-emberizidpasserine, Pomatostomus temporalis rubriceps,which occurssolely in the Andesof (from Edwards et al. 1991;GenBank Accession num- Colombia, Ecuador,and Peru. Many authors ber X60936). havehypothesized that closelyrelated species DNA isolationand sequencing.--DNAextracts were prepared from liver or muscletissue preserved in of North Americanbirds (Rand 1948,Mengel 95% ethanol or frozen at -80øC. Extractions were 1964, Hubbard 1973) and closelyrelated spe- performedusing either a 5% Chelexsolution (Walsh ciesof SouthAmerican birds (Haffer 1985) di- et al. 1991) or by NaC1 extraction (Miller et al. 1988). vergedfrom eachother as a result of isolation Usingstandard protocols (Burns 1997), specific frag- in refugia during Pleistoceneglaciation. The mentsof the cytochrome-bgene were then amplified biogeographichistory of Pirangaremains unex- usingthe polymerasechain reaction (PCR) and seven plored due to lack of knowledgeabout evolu- different primers: L14987, L15236, H15304, H15706 tionaryrelationships within this group. from Cicero and Johnson(1995); H15916 from Ed- Here, I use datafrom the cytochrome-bgene wards et al. (1991); H16065 from Smith and Patton (1993); and L15661 (ACCTCCTAGGAGA[C/ of themitochondria to reconstructthe first phy- T]CCAGA[C/A/T]AA[C/T]T), which is new to this logenetichypothesis for the genusPiranga. I study. Fragmentswere sequencedusing manual and then use the phylogenyto assesshow aspects ABI dye-terminator methods following standard of Piranga biology mentioned above have procedures(Burns 1997). SequenceNavigator Ver- changedduring the evolutionaryhistory of the sion 1.0.1 (Applied Biosystems,Perkin Elmer) was July1998] SystematicsofPiranga 623 ZZZ Z ZZ Z ZZZ OOZZZ 624 KEVINJ. BURNS [Auk, Vol. 115 used to reversecomplement opposing directions, to TABLE2. Plumagecharacters and character states of align differentfragments from the sameindividual, speciesof Piranga.• and to translate complete sequencesinto amino ac- ids. Character number Accuracyof DNA sequencingwas verified in four 111111 ways:(1) sequencingboth heavy and light strandsof Species 123456789012345 most PCR fragments, (2) using overlapping frag- Pirangaroseogularis 022320003331213 mentsof cytochromeb (approximately30% of theto- Pirangabidentata 112241111111111 tal sequenceis overlappedby two fragments),(3) se- Pirangafiava
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