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A Comprehensive Multilocus Phylogeny for the Wood-Warblers and a Revised Classification of the Parulidae (Aves) ⇑ Irby J

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Molecular Phylogenetics and Evolution 57 (2010) 753–770 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev A comprehensive multilocus phylogeny for the wood-warblers and a revised classification of the Parulidae (Aves) ⇑ Irby J. Lovette a, , Jorge L. Pérez-Emán b, John P. Sullivan a, Richard C. Banks c, Isabella Fiorentino a, Sergio Córdoba-Córdoba a,1, María 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 Zoología y Ecología 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 article info abstract Article history: The birds in the family Parulidae—commonly termed the New World warblers or wood-warblers—are a Received 2 March 2010 classic model radiation for studies of ecological and behavioral differentiation. Although the monophyly Revised 22 June 2010 of a ‘core’ wood-warbler clade is well established, no phylogenetic hypothesis for this group has Accepted 28 July 2010 included a full sampling of wood-warbler species diversity. We used parsimony, maximum likelihood, Available online 7 August 2010 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 Keywords: nucleotides) characters. The resulting phylogenetic hypotheses provide a highly congruent picture of Parulidae wood-warbler relationships, and indicate that the traditional generic classification of these birds recog- Wood-warbler Systematics nizes many non-monophyletic groups. We recommend a revised taxonomy in which each of 14 genera Phylogeny (Seiurus, Helmitheros, Mniotilta, Limnothlypis, Protonotaria, Parkesia, Vermivora, Oreothlypis, Geothlypis, Classification 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. Ó 2010 Elsevier Inc. All rights reserved. 1. Introduction in this otherwise well-studied radiation. Wood-warblers are small, primarily insectivorous birds with a broad diversity of habitat The wood-warblers of the avian family Parulidae have a long affinities and life-histories. Overall, the breeding distributions of history of serving as models for ecological and behavioral studies species in this New World group span the Arctic to temperate (e.g., MacArthur, 1958; Morse, 1970; Shutler and Weatherhead, South America, with centers of diversity in eastern North America, 1990; Price et al., 2000; Martin and Martin, 2001; Freckleton and the West Indies, Mexico and Central America, and Andean South Harvey, 2006; Lovette and Hochachka, 2006; Rabosky and Lovette, America. Most northern-breeding species are migratory, but many 2008), but there has been no comprehensive analysis of their phy- island and tropical species are sedentary or undertake only logenetic relationships that includes most of the genera or species 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 ⇑ Corresponding author. Fax: +1 607 254 2486. generally recognized 112–115 wood-warbler species distributed E-mail address: [email protected] (I.J. Lovette). 1 Present address: Department of Ecology and Evolutionary Biology, Princeton among 24–26 genera (Sibley and Monroe, 1990; Curson et al., University, Princeton, NJ 08544, USA. 1994; 1055-7903/$ - see front matter Ó 2010 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2010.07.018 754 I.J. Lovette et al. / Molecular Phylogenetics and Evolution 57 (2010) 753–770 AOU, 1998; Dickinson, 2003), but, as summarized below, recent species complexes (e.g., Bermingham et al., 1992; Klein and Brown, molecular phylogenetic studies have shown that 10 of these spe- 1994; Lovette et al., 1998; Buerkle, 1999; Lovette et al., 1999; Milá cies, representing seven genera, fall outside of a monophyletic et al., 2000; Zink et al., 2000; Lovette and Bermingham, 2001; ‘‘core Parulidae.” Kimura et al., 2002; Lovette, 2004; Markland and Lovette, 2005; Within the Passeriformes, the Parulidae fall within a highly di- Smith et al., 2005; Boulet and Gibbs, 2006; Milá et al., 2007; Col- verse group of songbirds often referred to as the New World nine- beck et al., 2008; Grus et al., 2009; McKay, 2009), and several pairs primaried oscines, although this term is somewhat of a misnomer of taxa that commonly hybridize have been investigated in com- as the tenth primary is reduced but not absent in the wood-war- plementary molecular and field studies (e.g., Rohwer et al., 2001; blers and most other members of this radiation (Hall, 2005). In Vallender et al., 2007; Irwin et al., 2009; Brelsford and Irwin, addition to the Parulidae, this larger group includes the traditional 2009). These investigations at the population/species interface families (sensu AOU, 1998) Coerebidae (Bananaquit), Thraupidae have helped define wood-warbler species and fostered inferences (tanagers), Emberizidae (emberizid sparrows and buntings), Cardi- about the biogeographic and ecological contexts of wood-warbler nalidae (cardinals, saltators, and allies), and Icteridae (blackbirds diversification. and allies). Recent molecular phylogenetic studies have revealed At an intermediate phylogenetic level within the Parulidae that many of these traditional families are not monophyletic, lead- radiation, three high-diversity groups have been the targets of ing to a series of revised classifications, some of which are still in phylogenetic studies that included all-or nearly all-constituent progress (e.g., Burns, 1997; Klicka et al., 2003; Klicka et al., 2007; species. The large genus Dendroica has many species that occur Alström et al., 2008; F.K. Barker, pers. comm.). There is strong in present-day sympatry; a historical pattern of early and rapid molecular phylogenetic support, however, for a monophyletic Dendroica radiation was first detected in phylogenies based on ‘‘core Parulidae” that includes all of the phenotypically typical mtDNA markers (Lovette and Bermingham, 1999), with later wood-warbler genera (Lovette and Bermingham, 2002; Klein reconstructions based on both mtDNA and nuclear markers simi- et al., 2004). larly supporting a pattern of density-dependent speciation in this In various recent studies encompassing a broad range of tax- group (Rabosky and Lovette, 2008). Pérez-Emán (2005) onomic and molecular marker sampling, the ‘‘core Parulidae” reconstructed relationships among the 12 species in the genus clade is consistently defined by a long basal internode separat- Myioborus using mtDNA sequence markers, and found that this ing it from all other taxa within the nine-primaried radiation group likely dispersed from Central America into South America, (Sibley and Ahlquist, 1990; Klicka et al., 2000; Lovette and where most of its subsequent diversification then occurred. Rela- Bermingham, 2002; Yuri and Mindell, 2002; Klein et al., 2004; tionships among the 13 species traditionally assigned to the clo- Klicka et al., 2007; Alström et al., 2008). Taxa traditionally clas- sely allied genera Oporornis and Geothlypis were recently sified within the wood-warblers but that are not members of reconstructed using mtDNA markers by Escalante et al. (2009), this core Parulidae clade include: (1) the Olive Warbler Peuced- who found gene-tree paraphyly between these genera as well as ramus taeniatus of North America, which on the basis of both among some populations of Geothlypis. morphological (e.g., Raikow, 1978) and molecular data (e.g., Previous studies that have addressed relationships across the Sibley and Ahlquist, 1990; Yuri and Mindell, 2002; Ericson and entire core Parulidae radiation include two allozyme-based surveys Johansson, 2003) is now placed in its own family and outside (Barrowclough and Corbin, 1978; Avise et al., 1980) that found rel- of the entire nine-primaried oscine assemblage; (2) the Yel- atively low differentiation among the species they compared, and low-breasted Chat Icteria virens of North America, the sole mem- which hence had modest phylogenetic resolution. Sibley and Ahl- ber of a lineage with variable placement close to the Icteridae, quist (1990) included only eight core Parulidae species from six Parulidae, or Emberizidae (e.g., Lovette and Bermingham, 2002; genera in their DNA–DNA hybridization-based phylogeny,
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