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Molecular Systematics and Biogeography of Antillean Thrashers, Tremblers, and Mockingbirds (Aves: Mimidae)

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Molecular Systematics and Biogeography of Antillean Thrashers, Tremblers, and Mockingbirds (Aves: Mimidae) The Auk 118(1):35-55, 2001 MOLECULAR SYSTEMATICS AND BIOGEOGRAPHY OF ANTILLEAN THRASHERS, TREMBLERS, AND MOCKINGBIRDS (AVES: MIMIDAE) JEFFREYS. HUNT, 1,3ELDREDGE BERMINGHAM, TM AND ROBERTE. RICKLEFS2 •SrnithsonianTropical Research Institute, Apartado 2072, Balboa,Republic of Panamd;and 2Departmentof Biology,University of Missouri-St.Louis, 8001 NaturalBridge Road, St. Louis, Missouri 63121-4499, USA ABSTRACT.--Weconstructed phylogenetic hypotheses for Greater and LesserAntillean Mimidae, including five endemicspecies of tremblersand thrashersthat representthe best plausibleexample of an avian radiation within the LesserAntilles. Phylogeneticrelation- shipswere inferred from analysisof 3,491base pairs (bp) of mitochondrialDNA (mtDNA) and roughly 780 bp of the nuclear-encodedmyoglobin gene. We used a subsetof mtDNA genesequences and pcrRFLPanalysis to evaluatethe phylogeographicrelationships among individualsrepresenting island populations of the Brown and Gray tremblers(Cinclocerthia ruficaudaand C. gutturalis), Pearly-eyedThrasher (Margaropsfuscatus), Scaly-breasted Thrasher(Margarops fuscus), and Antillean and continentalpopulations of the Tropical (Mi- musgilvus) and Northernmockingbirds (Mimus polyglottos). Phylogeographic analysis dis- tinguishedthree stronglydifferentiated mtDNA cladesamong tremblers, as well asdistinct southern(St. Lucia and Martinique)and northern(Dominica to Montserrat)mtDNA lineages of the Scaly-breastedThrasher. Minor geographicsubdivision was alsoobserved between continentaland Antillean populationsof the TropicalMockingbird. Phylogenetic analyses of species-levelMimidae relationshipsthat arebased on mtDNA and nuclearsequences pro- vide strongsupport for the monophylyand Antillean origin of a cladethat consistsof the tremblers,Pearly-eyed Thrasher, and Scaly-breastedThrasher, but rejectthe monophylyof the genusMargarops. Phylogenetic analysis cannot confirm the monophylyof all endemic Antillean mimids becauseof the apparentlycontemporaneous diversification of the Antil- lean White-breastedThrasher (Ramphocinclus brachyurus) with the continentalGray Catbird (Dumetellacarolinensis) and Black Catbird (Melanoptilaglabrirostris). However, an insertion and a deletionin the myoglobinintron 2 sequencesupport grouping the WestIndian thrash- ers and tremblers, from which we infer that the endemic Lesser Antillean mimids are an indigenousradiation. Assuming a constantmtDNA clockfor the Mimidae,the splittingof the Northernand Tropicalmockingbird lineages is roughlycontemporaneous with the sep- arationof the three tremblerclades, as well as the two Scaly-breastedThrasher clades. Ap- plicationof a mitochondrialDNA clockticking at 2% sequencedivergence per million years (Ma), suggeststhat the history of the endemicthrasher and tremblerlineage in the West Indies extendsback about 4 Ma, and the three distinct cladesof tremblerssplit about 2 Ma ago.Received 12 August1999, accepted 8 August2000. AMONG BIRDSof the West Indies, few endem- in thosegenera have partially overlappingdis- ic radiationshave resulted in sympatricdaugh- tributions in the Lesser Antilles, and four are ter species,and certainly none are comparable sympatricon the islandsof St. Lucia and Mar- to the radiations of Hawaiian honeycreepers tinique (Fig. 1). In the absenceof a mimid phy- (Drepanidinae)and Galapagosfin&es (Geos- logeny,however, it is not possibleto determine pizinae). In the LesserAntillean avifauna,the whether the Lesser Antillean mimid endemics three endemic Mimidae genera Margarops, are monophyleticand thus representan indig- Ramphocinclus,and Cinclocerthiaconstitute the enousradiation within that islandarchipelago. bestplausible example of an autochthonousra- The principal objectiveof this study was to diation. The five currentlyrecognized species providea phylogenetichypothesis for the gen- era of mimids found within the Caribbean Ba- sin and assess whether the endemic Lesser An- 3 Present address: Bird Division, Field Museum of Natural History,Roosevelt Road at LakeShore Drive, tillean taxa were producedwithin the islands Chicago,Illinois 60605,USA or representmultiple colonizationsfrom the 4 E-mail: [email protected] American continents. In addition to the endem- 35 36 HUNT,BERMINGHAM, AND RICKLEFS [Auk,Vol. 118 Finally,our analysesprovide a molecular-sys- tematicperspective on the taxonomicstatus of Cinclocerthiaand Margaropsand on the evolu- tionary status of subspeciesin both these genera. We sequencedthe full mitochondrialATP synthase6 and 8 genesfor two or more indi- Lesser Antilles viduals representingall speciesand multiple geographicpopulations of Lesser Antillean mimids. Phylogeneticanalysis of the ATPase ß - C/nclocerthlaspecies SLI• ßß00 sequencesformed the basis of our biogeo- ß - Margarops(Allen/a) fuscus • - Margaropsfuscatus sv 4 graphicappraisal of the two Margaro?sspecies, ß - Ramphocinc/usbrachyurus Cinclocerthia,and the two widespreadMirnus # species.Mitochondrial genotypes were also de- termined for additional Margaro?sfuscus and M. fuscatusindividuals using RFLP analysisof PCR-amplifiedATPase fragments. Following our initial phylogeneticanalyses of Caribbean mimids, we selected11 species (including out- groups) and a secondgenetically differentiated FIG. 1. The geographicdistribution of the four population of C. ruficaudafor a more detailed speciesof thrashersand tremblers(Mimidae) found in the LesserAntilles. Specimensincluded in this molecular-systematicanalysis. Our phyloge- study were collectedfrom islandsrepresented by the netichypothesis for Caribbeanmimid relation- filled symbols.Geographic abbreviations are as fol- shipsis basedon direct sequenceanalysis of lows: Puerto Rico (PR), Barbuda(BU), Antigua (AN), 3,491 base pairs (bp) of mitochondrialDNA Montserrat(MO), Guadeloupe(GU), Dominica(DO), (mtDNA) and approximately780 bp that rep- Martinique (MA), St. Lucia (SL), and St. Vincent resentthe nuclear-encodedmyoglobin intron 2 (SV). and shortregions of flankingexons 2 and 3. STUDY AREA AND TAXA ic thrashersand tremblers,our phylogenetic analysisincludes the migratory Gray Catbird The LesserAntilles (Fig. 1) comprisea corechain (Dumetellacarolinensis) of North America, the of six medium-sized, volcanic, oceanic islands with Black Catbird (Melano?tila glabrirostris)of high elevationand considerableenvironmental het- northernCentral America,the Blue Mocking- erogeneity (Grenada, St. Vincent, St. Lucia, Marti- bird (Melanotis caerulescens)of Mexico, and nique, Dominica, and Guadeloupe).Several smaller three Caribbean-basinspecies of mockingbird islandsare distributedamong the corechain includ- (Mimus;Fig. 2). Our taxonomicsampling of the ing a group of smaller, more northerly volcanicis- landsthat havehigh elevations(Montserrat through Mimidae includedToxostorna (T. rufurnand T. ci- Saba),and an outer chainof low-lying,dry islands, nereurn)and Oreosco?tesrnontanus, but our ini- that consistof uplifted marine sediments,also to the tial molecular-systematicresults indicated that north (the easternhalf of Guadeloupethrough An- Dumetellaand Melano?tilaare closerrelatives of guilla). The Lesser Antilles, excluding Barbados, the Antillean-endemic thrashers and tremblers. achievedtheir presentgeographic configuration by Accordingly, we deleted Toxostomaand Oreos- the middle of the Miocene,at least15 Ma ago (Don- coptesfrom the presentanalysis. nelly 1985, 1989, Iturralde-Vinent and MacPhee The secondobjective of this study was to 1999). providea phylogeographicdescription of each Weconsider the LesserAntillean archipelago to be WestIndian mimid speciesfor which we have considerablyolder than its contemporaryavifauna (Ricklefsand Bermingham1999). Nonetheless,the moderatesamples and broad geographicrep- West Indian thrashers and tremblers are so distinc- resentation.These species are the Scaly-breast- tive that early workersgrouped them variously with ed Thrasher (Margaropsfuscus), Pearly-eyed the ant thrushes, ovenbirds, wrens, and thrushes Thrasher(M. fuscatus),Brown Trembler(Cin- (seeGulledge 1975). By the beginningof the twen- clocerthiaruficauda), Gray Trembler (C. guttur- tieth century, ornithologistshad reachedgeneral alis),and Tropical and Northern mockingbirds. agreementon groupingthe Antilleanforms together January2001] CaribbeanMimidae Systematics 37 us • BH West Indies M. polyglottos I I M. gundlachii DO• MA• SL--t M. gilvus sv• VE TR Flo. 2. The geographicdistribution of the threespecies of mockingbirds(Mimus) found in theWest Indies. Linesindicate the southernextent of Mimuspolyglottos and the northernextent of M. gilvusin the Antilles. Mimusgundlachii is foundon the BahamaIslands and keysoff the northerncoast of Cubain additionto the Jamaicandistribution pictured. Geographic abbreviations are asfollows: United States (US), Bahamas (BH), Jamaica(JA) Dominican Republic (RD), Puerto Rico (PR), Dominica (DO), Martinique (MA), St. Lucia (SL), St. Vincent (SV), Grenada (GR), Trinidad (TR), and Venezuela (VE). with othermimids as a separatefamily, the Mimidae. of Bermuda and winters to the south in Central Nevertheless,the positionof the Antilleanthrashers America and the Greater Antilles (AOU 1983). The and tremblerswithin that family,their relationships Black Catbird has a Caribbean-slopedistribution to eachother, and diversificationof eachof the spe- from northern Honduras to Yucatan, Mexico (AOU ciesamong islands are still poorly understood. 1983). Our molecular-systematic analysis was Margaropsand Alleniahave always been grouped roundedout with the mockingbirdsof the genusMi- togetherand, indeed,are
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