A comprehensive multilocus phylogeny for the wood-warblers and a revised classification of the Parulidae (Aves) Irby J. Lovette a,���, Jorge L. P��rez-Em��n b, John P. Sullivan a, Richard C. Banks c, Isabella Fiorentino a, Sergio C��rdoba-C��rdoba a,1, Mar��a Echeverry-Galvis a,1, F. Keith Barker d, Kevin J. Burns e, John Klicka f, Scott M. Lanyon d, Eldredge Bermingham g a Fuller Evolutionary Biology Program, Cornell Lab of Ornithology, Cornell University, 159 Sapsucker Woods Road, Ithaca, NY 14950, USA b Instituto de Zoolog��a y Ecolog��a Tropical, Universidad Central de Venezuela, Apartado Postal 47058, Caracas 1041-A, Venezuela c United States Geological Survey, Patuxent Wildlife Research Center, National Museum of Natural History, Washington, DC 20013, USA d Bell Museum of Natural History, University of Minnesota, St. Paul, MN 55108, USA e Department of Biology, San Diego State University, San Diego, CA 92182, USA f Barrick Museum of Natural History, University of Nevada, Las Vegas, NV 89154, USA g Smithsonian Tropical Research Institute, Balboa, Panama a r t i c l e i n f o Article history: Received 2 March 2010 Revised 22 June 2010 Accepted 28 July 2010 Available online 7 August 2010 Keywords: Parulidae Wood-warbler Systematics Phylogeny Classification a b s t r a c t The birds in the family Parulidae���commonly termed the New World warblers or wood-warblers���are a classic model radiation for studies of ecological and behavioral differentiation. Although the monophyly of a ���core��� wood-warbler clade is well established, no phylogenetic hypothesis for this group has included a full sampling of wood-warbler species diversity. We used parsimony, maximum likelihood, and Bayesian methods to reconstruct relationships among all genera and nearly all wood-warbler species, based on a matrix of mitochondrial DNA (5840 nucleotides) and nuclear DNA (6 loci, 4602 nucleotides) characters. The resulting phylogenetic hypotheses provide a highly congruent picture of wood-warbler relationships, and indicate that the traditional generic classification of these birds recog- nizes many non-monophyletic groups. We recommend a revised taxonomy in which each of 14 genera (Seiurus, Helmitheros, Mniotilta, Limnothlypis, Protonotaria, Parkesia, Vermivora, Oreothlypis, Geothlypis, Setophaga, Myioborus, Cardellina, Basileuterus, Myiothlypis) corresponds to a well-supported clade these nomenclatural changes also involve subsuming a number of well-known, traditional wood-warbler gen- era (Catharopeza, Dendroica, Ergaticus, Euthlypis, Leucopeza, Oporornis, Parula, Phaeothlypis, Wilsonia). We provide a summary phylogenetic hypothesis that will be broadly applicable to investigations of the his- torical biogeography, processes of diversification, and evolution of trait variation in this well studied avian group. �� 2010 Elsevier Inc. All rights reserved. 1. Introduction The wood-warblers of the avian family Parulidae have a long history of serving as models for ecological and behavioral studies (e.g., MacArthur, 1958 Morse, 1970 Shutler and Weatherhead, 1990 Price et al., 2000 Martin and Martin, 2001 Freckleton and Harvey, 2006 Lovette and Hochachka, 2006 Rabosky and Lovette, 2008), but there has been no comprehensive analysis of their phy- logenetic relationships that includes most of the genera or species in this otherwise well-studied radiation. Wood-warblers are small, primarily insectivorous birds with a broad diversity of habitat affinities and life-histories. Overall, the breeding distributions of species in this New World group span the Arctic to temperate South America, with centers of diversity in eastern North America, the West Indies, Mexico and Central America, and Andean South America. Most northern-breeding species are migratory, but many island and tropical species are sedentary or undertake only short-distance elevational migrations. The wood-warblers breed exclusively in the New World, and they are not closely allied to the various Old World songbirds (from 10 or more families) that are also commonly termed ������warblers.��� Modern classifications have generally recognized 112���115 wood-warbler species distributed among 24���26 genera (Sibley and Monroe, 1990 Curson et al., 1994 1055-7903/$ - see front matter �� 2010 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2010.07.018 ��� Corresponding author. Fax: +1 607 254 2486. E-mail address: IJL2@cornell.edu (I.J. Lovette). 1 Present address: Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ 08544, USA. Molecular Phylogenetics and Evolution 57 (2010) 753���770 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev

AOU, 1998 Dickinson, 2003), but, as summarized below, recent molecular phylogenetic studies have shown that 10 of these spe- cies, representing seven genera, fall outside of a monophyletic ������core Parulidae.��� Within the Passeriformes, the Parulidae fall within a highly di- verse group of songbirds often referred to as the New World nine- primaried oscines, although this term is somewhat of a misnomer as the tenth primary is reduced but not absent in the wood-war- blers and most other members of this radiation (Hall, 2005). In addition to the Parulidae, this larger group includes the traditional families (sensu AOU, 1998) Coerebidae (Bananaquit), Thraupidae (tanagers), Emberizidae (emberizid sparrows and buntings), Cardi- nalidae (cardinals, saltators, and allies), and Icteridae (blackbirds and allies). Recent molecular phylogenetic studies have revealed that many of these traditional families are not monophyletic, lead- ing to a series of revised classifications, some of which are still in progress (e.g., Burns, 1997 Klicka et al., 2003 Klicka et al., 2007 Alstr��m et al., 2008 F.K. Barker, pers. comm.). There is strong molecular phylogenetic support, however, for a monophyletic ������core Parulidae��� that includes all of the phenotypically typical wood-warbler genera (Lovette and Bermingham, 2002 Klein et al., 2004). In various recent studies encompassing a broad range of tax- onomic and molecular marker sampling, the ������core Parulidae��� clade is consistently defined by a long basal internode separat- ing it from all other taxa within the nine-primaried radiation (Sibley and Ahlquist, 1990 Klicka et al., 2000 Lovette and Bermingham, 2002 Yuri and Mindell, 2002 Klein et al., 2004 Klicka et al., 2007 Alstr��m et al., 2008). Taxa traditionally clas- sified within the wood-warblers but that are not members of this core Parulidae clade include: (1) the Olive Warbler Peuced- ramus taeniatus of North America, which on the basis of both morphological (e.g., Raikow, 1978) and molecular data (e.g., Sibley and Ahlquist, 1990 Yuri and Mindell, 2002 Ericson and Johansson, 2003) is now placed in its own family and outside of the entire nine-primaried oscine assemblage (2) the Yel- low-breasted Chat Icteria virens of North America, the sole mem- ber of a lineage with variable placement close to the Icteridae, Parulidae, or Emberizidae (e.g., Lovette and Bermingham, 2002 Yuri and Mindell, 2002 Klein et al., 2004 Klicka et al., 2007) (3) three species of Neotropical chats in the genus Granatellus (Lovette and Bermingham, 2002), which fall within a group re- cently recognized as cardinal-grosbeaks (Klicka et al., 2007) (4) the Wrenthrush Zeledonia coronata of southern Central America, which like Icteria represents an old lineage that falls outside���but possibly close to���the core Parulidae (Lovette and Bermingham 2002 Klicka et al., 2007) (5) the Green-tailed Warbler Microligea palustris and the White-winged Warbler Xenoligea montana, two sister-taxa endemic to the island of His- paniola, which are likely allied to a small group of other rela- tively old West Indian-endemic lineages such as Phaenicophilus (Lovette and Bermingham, 2002 Klein et al., 2004 Klicka et al., 2007) and (6) two species of Teretistris warblers endemic to Cuba, which likewise appear to have affinities with other non- parulid taxa from the West Indies (Lovette and Bermingham, 2002 Klein et al., 2004 Klicka et al., 2007). Although the deeper relationships of these various lineages are not yet well resolved, the strong and replicated evidence for a well-supported and monophyletic core Parulidae allows us to focus here on recon- structing phylogenetic relationships within this more recently derived group. Our understanding of phylogenetic relationships within the core Parulidae clade is variable, because only some subsets of the radiation have been sampled intensively with informative markers. Phylogeographic studies have been conducted on many species or species complexes (e.g., Bermingham et al., 1992 Klein and Brown, 1994 Lovette et al., 1998 Buerkle, 1999 Lovette et al., 1999 Mil�� et al., 2000 Zink et al., 2000 Lovette and Bermingham, 2001 Kimura et al., 2002 Lovette, 2004 Markland and Lovette, 2005 Smith et al., 2005 Boulet and Gibbs, 2006 Mil�� et al., 2007 Col- beck et al., 2008 Grus et al., 2009 McKay, 2009), and several pairs of taxa that commonly hybridize have been investigated in com- plementary molecular and field studies (e.g., Rohwer et al., 2001 Vallender et al., 2007 Irwin et al., 2009 Brelsford and Irwin, 2009). These investigations at the population/species interface have helped define wood-warbler species and fostered inferences about the biogeographic and ecological contexts of wood-warbler diversification. At an intermediate phylogenetic level within the Parulidae radiation, three high-diversity groups have been the targets of phylogenetic studies that included all-or nearly all-constituent species. The large genus Dendroica has many species that occur in present-day sympatry a historical pattern of early and rapid Dendroica radiation was first detected in phylogenies based on mtDNA markers (Lovette and Bermingham, 1999), with later reconstructions based on both mtDNA and nuclear markers simi- larly supporting a pattern of density-dependent speciation in this group (Rabosky and Lovette, 2008). P��rez-Em��n (2005) reconstructed relationships among the 12 species in the genus Myioborus using mtDNA sequence markers, and found that this group likely dispersed from Central America into South America, where most of its subsequent diversification then occurred. Rela- tionships among the 13 species traditionally assigned to the clo- sely allied genera Oporornis and Geothlypis were recently reconstructed using mtDNA markers by Escalante et al. (2009), who found gene-tree paraphyly between these genera as well as among some populations of Geothlypis. Previous studies that have addressed relationships across the entire core Parulidae radiation include two allozyme-based surveys (Barrowclough and Corbin, 1978 Avise et al., 1980) that found rel- atively low differentiation among the species they compared, and which hence had modest phylogenetic resolution. Sibley and Ahl- quist (1990) included only eight core Parulidae species from six genera in their DNA���DNA hybridization-based phylogeny, in which they form a distinct clade with low internal resolution. More re- cently, Lovette and Bermingham (2002) included 30 species in 19 core Parulidae genera in reconstructions based on robust sampling of mtDNA loci and one nuclear locus Klein et al. (2004) recon- structed relationships among 47 core Parulidae species from 15 genera using mtDNA cytochrome b sequences and Lovette and Ho- chachka (2006) generated a mtDNA-based phylogeny as part of a study of the ecological interactions of 43 North American wood- warbler species from 12 genera. Considered together, these se- quence-based studies have helped clarify the relationships of some Parulidae lineages, but they have also suggested that the core Parul- idae diversified in successive waves of radiation, that most tradi- tional parulid genera do not represent monophyletic groups, and that a well-informed revision of wood-warbler classification will require reconstructions based on robust sampling of both markers and species. The goal of the present study is to present a comprehensive phylogenetic treatment of the entire Parulidae radiation based on nearly complete species-level sampling and an informative set of both mitochondrial and nuclear sequence markers. The resulting phylogenetic reconstructions have high utility for revising the gen- eric taxonomy of the Parulidae, for additional model-based explo- rations of patterns and processes of its diversification, and in comparative analyses that explore the drivers of differentiation in morphological, ecological, and behavioral traits for which this group is well known. 754 I.J. Lovette et al. /Molecular Phylogenetics and Evolution 57 (2010) 753���770

Table 1 Taxa included in this study, museum source information, and a proposed new generic classification of the Parulidae. Taxon English Name Recommended Museum source Tissue Collection locality Genusa Informationb Typec Seiurus aurocapilla Ovenbird Seiurus STRI-PRSAU1 T Puerto Rico, Patillas Helmitheros vermivorus Worm-eating Warbler Helmitheros STRI-JAHVE2 T Jamaica, St. Andrews Parish, John Crow Nat. Park Seiurus motacilla Louisiana Waterthrush Parkesia STRI-JASMT1 T Jamaica, Westmoreland Parish, Savanna la Mar Seiurus noveboracensis Northern Waterthrush Parkesia STRI-HASNO144 T Honduras, Cayos Cochinos, Cochino Pequeno Vermivora bachmanii Bachman���s Warbler Vermivora AMNH-759214 aDNA USA, South Carolina St., Charleston, I���on Swamp (1915) Vermivora chrysoptera Golden-winged Warbler Vermivora CUMV-44030 T USA, New York St., Tompkins County Vermivora pinusd Blue-winged Warbler Vermivora CUMV-228087252 T USA, New York St., Tompkins County Mniotilta varia Black-and-white Warbler Mniotilta STRI-JAMVA2 T Jamaica, St. Andrews Parish, John Crow Nat. Park Protonotaria citrea Prothonotary Warbler Protonotaria LSUMNS-B23575 T USA, Louisiana St., St. Martin Parish Limnothlypis swainsonii Swainson���s Warbler Limnothlypis STRI-JALSW2 T Jamaica, St. Andrews Parish, John Crow Nat. Park Parula gutturalis Flame-throated Warbler Oreothlypis LSUMNS-B26458 T Panama, Chiriqui Province, Boquete Parula superciliosa Crescent-chested Warbler Oreothlypis FMNH-5730-BMM154 T Mexico, Est. Michoacan, Cerro de Tancitaro Vermivora peregrina Tennessee Warbler Oreothlypis STRI-HAVPE62 T Honduras, Dept. Atl��ntida, La Ceiba Vermivora celata Orange-crowned Warbler Oreothlypis UWBM-53827 T USA, Alaska St., Valdez-Cordova County, Valdez Vermivora crissalis Colima Warbler Oreothlypis FMNH-395824 T Mexico, Est. Mexico, Ocuilan Vermivora luciae Lucy���s Warbler Oreothlypis ANSP-GFB1920 T USA, Arizona, Cochise County Vermivora virginiae Virginia���s Warbler Oreothlypis UNLVBMNH- MBM10245 T USA, Nevada St., Clark County Vermivora ruficapilla Nashville Warbler Oreothlypis UWBM-49896 T USA, Washington St., Yakima County, Mt. Adams Oporornis agilis Connecticut Warbler Geothlypis UMBM-JK97004 T USA, Minnesota St., Washington County Leucopeza semperi Semper���s Warbler Geothlypis ANSP-507561 aDNA St Lucia (collection year undocumented) Geothlypis aequinoctialis Masked Yellowthroat Geothlypis CUMV-50367 T Uruguay, Dept. Artigas, Arroyo Mandiyu Geothlypis poliocephala Gray-crowned Yellowthroat Geothlypis CUMV-36479 aDNA Mexico, Est. Chiapas, Berrio Zaibol (1966) Oporornis tolmiei MacGillivray���s Warbler Geothlypis UWBM-CDS4192 T USA, Washington, Whatcom, Mt. Baker Oporornis philadelphia Mourning Warbler Geothlypis CUMV-228087288 T USA, New York St., Tompkins County Oporornis formosus Kentucky Warbler Geothlypis STRI-PROFO1 T Puerto Rico, Carite State Forest Geothlypis semiflava Olive-crowned Yellowthroat Geothlypis CUMV-IJL04130 T Panama, Prov. Bocas del Toro, Chiriqui Grande Geothlypis speciosa Black-polled Yellowthroat Geothlypis CUMV-33368 aDNA Mexico, Est. Guanajuato, Lago Yuriria (1964) Geothlypis beldingi Belding���s Yellowthroat Geothlypis CUMV-16802 aDNA Mexico, Est. Baja California Sur, San Jose del Cabo (1887) Geothlypis rostrata Bahama Yellowthroat Geothlypis STRI-ABGRO1 T Bahamas, Abaco Island Geothlypis flavovelata Altamira Yellowthroat Geothlypis CUMV-11635 aDNA Mexico, Est. Tamaulipas, Alta Mira (1941) Geothlypis trichas Common Yellowthroat Geothlypis STRI-JAGTR1 T Jamaica, St. Andrews Parish, John Crow Nat. Park Geothlypis nelsoni Hooded Yellowthroat Geothlypis CUMV-29306 aDNA Mexico, Est. Puebla, Mt. Malinche (1954) Catharopeza bishopi Whistling Warbler Setophaga STRI-SVCBI5 T St. Vincent, Cumberland Valley Dendroica plumbea Plumbeous Warbler Setophaga STRI-DODPL1 T Dominica, Springfield Dendroica angelae Elfin-woods Warbler Setophaga LSUMNS-B11325 T Puerto Rico, Maricao State Forest Dendroica pharetra Arrow-headed Warbler Setophaga STRI-JADPH6 T Jamaica, St. Andrews Parish, John Crow Nat. Park Wilsonia citrina Hooded Warbler Setophaga CUMV-50468 T USA, New York St., Monroe County Setophaga ruticilla American Redstart Setophaga STRI-JASRU1 T Jamaica, St. Andrews Parish, John Crow Nat. Park Dendroica kirtlandii Kirtland���s Warbler Setophaga USNM-B06558- 613582 T USA, Michigan, Oscoda County Dendroica tigrina Cape May Warbler Setophaga STRI-JADTI1 T Jamaica, St. Elizabeth Parish, Luana Point Dendroica cerulea Cerulean Warbler Setophaga LSUMNS-B3397 T USA, Louisiana St., Cameron Parish Parula americana Northern Parula Setophaga STRI-JAPAM1 T Jamaica, St. Elizabeth Parish, Luana Point Parula pitiayumi Tropical Parula Setophaga LSUMNS-B2150 T Panama, Prov. Darien, Cana Dendroica magnolia Magnolia Warbler Setophaga CUMV-44183 T USA, New York St., Monroe County Dendroica castanea Bay-breasted Warbler Setophaga STRI-HA147 T Honduras, Cayos Cochinos, Cochino Pequeno Dendroica fusca Blackburnian Warbler Setophaga ANSP-B2011 T Ecuador, Prov. Esmeraldas Dendroica petechia Yellow Warbler Setophaga LSUMNS-B20611 T USA, Louisiana St., Cameron Parish Dendroica pensylvanica Chestnut-sided Warbler Setophaga CUMV-50271 T USA, New York St., Tompkins County Dendroica striata Blackpoll Warbler Setophaga ANSP-B3659 T USA, Pennsylvania St., Bucks County Dendroica caerulescens Black-throated Blue Warbler Setophaga STRI-JADCR1 T Jamaica, St. Andrews Parish, John Crow Nat. Park Dendroica palmarum Palm Warbler Setophaga LSUMNS-B21581 T USA, California St., San Bernardino County Dendroica pityophila Olive-capped Warbler Setophaga STRI-ABDPY1 T Bahamas, Abaco Island Dendroica pinus Pine Warbler Setophaga ANSP-B2933 T USA, New Jersey St., Cumberland County Dendroica coronata Yellow-rumped Warbler Setophaga STRI-RDDCO1 T Dominican Republic, Prov. La Vega, Valle Nuevo Dendroica dominica Yellow-throated Warbler Setophaga LSUMNS-B3386 T USA, Louisiana St., Cameron Parish Dendroica discolor Prairie Warbler Setophaga STRI-JADDI2 T Jamaica, St. Elizabeth Parish, Luana Point Dendroica vitellina Vitelline Warbler Setophaga STRI-GCDVI129 T Cayman Islands, Grand Cayman Dendroica adelaidae Adelaide���s Warbler Setophaga STRI-PRDAD2 T Puerto Rico, Guanica Dendroica subita Barbuda Warbler Setophaga STRI-BUDAD1 T Barbuda, Martello Tower Dendroica delicata St. Lucia Warbler Setophaga STRI-SLDAD10 T St. Lucia, Babonneau, Anse Sorciere Dendroica graciae Grace���s Warbler Setophaga LSUMNS-B10176 T USA, Arizona, Santa Cruz County Dendroica nigrescens Black-throated Gray Warbler Setophaga UWBM-CSW3126/ 52347 T USA, Washington St., Lewis County Dendroica occidentalis Hermit Warbler Setophaga UWBM-CSW2920/ 46693 T USA, California St., Sierra County Dendroica townsendi Townsend���s Warbler Setophaga UWBM-CSW2539/ 41918 T USA, Washingon St., Pend Oreille County (continued on next page) I.J. 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