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A Comprehensive Species-Level Molecular Phylogeny of the New World

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A Comprehensive Species-Level Molecular Phylogeny of the New World YMPEV 4758 No. of Pages 19, Model 5G 2 December 2013 Molecular Phylogenetics and Evolution xxx (2013) xxx–xxx 1 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev 5 6 3 A comprehensive species-level molecular phylogeny of the New World 4 blackbirds (Icteridae) a,⇑ a a b c d 7 Q1 Alexis F.L.A. Powell , F. Keith Barker , Scott M. Lanyon , Kevin J. Burns , John Klicka , Irby J. Lovette 8 a Department of Ecology, Evolution and Behavior, and Bell Museum of Natural History, University of Minnesota, 100 Ecology Building, 1987 Upper Buford Circle, St. Paul, MN 9 55108, USA 10 b Department of Biology, San Diego State University, San Diego, CA 92182, USA 11 c Barrick Museum of Natural History, University of Nevada, Las Vegas, NV 89154, USA 12 d Fuller Evolutionary Biology Program, Cornell Lab of Ornithology, Cornell University, 159 Sapsucker Woods Road, Ithaca, NY 14950, USA 1314 15 article info abstract 3117 18 Article history: The New World blackbirds (Icteridae) are among the best known songbirds, serving as a model clade in 32 19 Received 5 June 2013 comparative studies of morphological, ecological, and behavioral trait evolution. Despite wide interest in 33 20 Revised 11 November 2013 the group, as yet no analysis of blackbird relationships has achieved comprehensive species-level sam- 34 21 Accepted 18 November 2013 pling or found robust support for most intergeneric relationships. Using mitochondrial gene sequences 35 22 Available online xxxx from all 108 currently recognized species and six additional distinct lineages, together with strategic 36 sampling of four nuclear loci and whole mitochondrial genomes, we were able to resolve most relation- 37 23 Keywords: ships with high confidence. Our phylogeny is consistent with the strongly-supported results of past stud- 38 24 Blackbird ies, but it also contains many novel inferences of relationship, including unexpected placement of some 39 25 Classification 26 Icteridae newly-sampled taxa, resolution of relationships among major clades within Icteridae, and resolution of 40 27 Phylogeny genus-level relationships within the largest of those clades, the grackles and allies. We suggest taxonomic 41 28 Systematics revisions based on our results, including restoration of Cacicus melanicterus to the monotypic Cassiculus, 42 29 Taxonomy merging the monotypic Ocyalus and Clypicterus into Cacicus, restoration of Dives atroviolaceus to the 43 30 monotypic Ptiloxena, and naming Curaeus forbesi to a new monotypic genus, Anumara. Our hypothesis 44 of blackbird phylogeny provides a foundation for ongoing and future evolutionary analyses of the group. 45 Ó 2013 Elsevier Inc. All rights reserved. 46 47 48 49 1. Introduction song divergence (Price and Lanyon, 2002b, 2004a; Price et al., 67 2007), migration (Kondo and Omland, 2007), biogeographic history 68 50 The New World blackbirds (Icteridae) are among the best (Sturge et al., 2009), and ecological niche divergence (Eaton et al., 69 51 known and studied songbirds, both through exemplar species such 2008). 70 52 as the Red-winged Blackbird (Agelaius phoeniceus) and collectively Knowledge of phylogeny is a prerequisite for comparative 71 53 as a model clade in numerous studies of morphological, ecological, analysis and the basis for systematic classification, but past analy- 72 54 and behavioral trait evolution. The size of the family (108 ses of blackbird relationships lacked comprehensive species-level 73 55 species) and its variability along several dimensions of general the- sampling and failed to find robust support for most intergeneric 74 56 oretical interest makes Icteridae especially attractive for compara- relationships. The first molecular phylogenies of Icteridae with 75 57 tive studies. Topics that have been investigated comparatively in broad taxonomic sampling provided revolutionary insights into 76 58 blackbirds include mating systems (Searcy et al., 1999), brood par- relationships within the family (Lanyon, 1994; Freeman and Zink, 77 59 asitism (Lanyon, 1992), sexual size dimorphism (Webster, 1992), 1995; Lanyon and Omland, 1999) and its subgroups (Johnson and 78 60 sexual dichromatism (Irwin, 1994; Hofmann et al., 2008a, 2008b; Lanyon, 1999; Omland et al., 1999; Price and Lanyon, 2002a, 79 61 Friedman et al., 2009), plumage pattern divergence (Omland and 2004a; Barker et al., 2008). Those findings were a huge advance 80 62 Lanyon, 2000; Price and Whalen, 2009), chemical bases of plumage over the diffuse hypotheses of relationship presented in taxonomic 81 63 Q2 color (Hofmann et al., 2006, 2007, 2008a, 2008b; Friedman et al., reviews based on informal evaluation of the external anatomy of 82 64 2011), ultraviolet and structural color (Eaton, 2006; Shawkey museum skins (e.g. Ridgway, 1902; Hellmayr, 1937; Blake, 1968) 83 65 et al., 2006), ecological correlates of plumage color (Johnson and or very limited molecular sampling (e.g. Sibley and Monroe, 84 66 Lanyon, 2000) and female song (Price, 2009; Price et al., 2009), 1990). Sequence-based molecular studies, for the first time, 85 brought together large numbers of informative characters with 86 objective analytical methods to resolve relationships among most 87 ⇑ Corresponding author. Fax: +1 612 624 6777. species and clades, tasks for which morphological characteristics 88 E-mail address: [email protected] (A.F.L.A. Powell). 1055-7903/$ - see front matter Ó 2013 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ympev.2013.11.009 Please cite this article in press as: Powell, A.F.L.A., et al. A comprehensive species-level molecular phylogeny of the New World blackbirds (Icteridae). Mol. Phylogenet. Evol. (2013), http://dx.doi.org/10.1016/j.ympev.2013.11.009 YMPEV 4758 No. of Pages 19, Model 5G 2 December 2013 2 A.F.L.A. Powell et al. / Molecular Phylogenetics and Evolution xxx (2013) xxx–xxx 89 had proven to be weakly informative (e.g. Björklund, 1991)or Key objectives were as follows: (1) sample all currently-recognized 155 90 even—in combination with informal and speculative methods of species not included in previous studies; (2) robustly resolve rela- 156 91 inference—misleading (e.g. Beecher, 1950, 1951). tionships among major clades within Icteridae; (3) robustly resolve 157 92 In contrast to the other diverse families within the New World relationships among the grackles and allies, especially within a 158 93 nine-primaried oscine clade—namely, the tanagers (Thraupidae), phenotypically and ecologically diverse clade of South American 159 94 cardinal-grosbeaks (Cardinalidae), New World sparrows (Ember- endemics, which previous studies failed to resolve with confi- 160 95 izidae), and wood-warblers (Parulidae)—among which many spe- dence; (4) compare patterns of relationship found in previous 161 96 cies and genera have recently been shuffled, the constitution of mitochondrial studies to results from nuclear loci, and (5) suggest 162 97 Icteridae has been unaffected by results from molecular phyloge- taxonomic revisions based on our results. Preliminary results from 163 98 netic studies (e.g. Burns, 1997; Klicka et al., 2000, 2007; Burns this project (i.e. phylogenies inferred from less comprehensive 164 99 et al., 2002, 2003; Lovette and Bermingham, 2002; Yuri and versions of our dataset) have already informed studies of female 165 100 Mindell, 2002; Klein et al., 2004; Alström et al., 2008; Lovette song (Price, 2009; Price et al., 2009) and plumage color evolution 166 101 et al., 2010; Barker et al., 2013). Apparently, features that have (Friedman et al., 2011). 167 102 traditionally been used to recognize blackbirds such as bill shape 103 (e.g. casque of maxilla; see Webster, 2003), morphology related 104 to gape-feeding by many species (Beecher, 1951; Orians, 1985), 2. Methods 168 105 and general similarities in shape, plumage, voice, display, and 106 ecology, have led to their accurate diagnosis. The only contrary 2.1. Taxon and character sampling 169 107 assertions have been the following: (1) placement of Spiza in 108 Icteridae (Beecher, 1951; Raikow, 1978), which was immediately Our analyses encompassed 114 ingroup and four outgroup taxa 170 109 disputed (see e.g. Tordoff, 1954) and is not currently supported (Table 1). Sampling within Icteridae included all species currently 171 110 (e.g. molecular evidence places Spiza deep within the Cardinalidae; recognized by taxonomic authorities (Dickinson, 2003; Remsen 172 111 Klicka et al., 2007); (2) unsubstantiated suggestions of affinity et al., 2012; Gill and Donsker, 2012) or in prominent references 173 112 between Compsothraupis loricata and Icteridae (Jaramillo and (Jaramillo and Burke, 1999; Fraga, 2011) except that we did not ob- 174 113 Burke, 1999); and (3) lack thereof for Amblycercus (Fraga, 2011). tain samples of Psarocolius b. bifaciatus, Agelaioides badius fringilla- 175 114 Comprehensive genus-level multi-locus molecular sampling of rius and Molothrus aeneus armenti (see also Dugand and 176 115 the nine-primaried oscines strongly supports the monophyly of Eisenmann, 1983) and we chose not to include samples of Psaroco- 177 116 Icteridae (Barker et al., 2013) as traditionally defined. lius angustifrons alfredi (see Section 4.4) and Agelaius phoeniceus 178 117 Although molecular phylogenetic studies of Icteridae (e.g. gubernator (see Dufort and Barker, 2013). About 10% of the sam- 179 118 Lanyon, 1992, 1994; Freeman and Zink, 1995; Lanyon and Omland, pled taxa had not been included in previous molecular phylogenies 180 119 1999) did not lead to its redefinition, they shed considerable light of Icteridae, including three meadowlarks (Sturnella militaris, S. loy- 181 120 on relationships within the family, including recognition of constit- ca, S. defilippii), three caciques and oropendolas (Cacicus koepckeae, 182 121 uent clades and discovery that several genera—Molothrus, Agelaius, Psarocolius cassini, P. guatimozinus), an oriole (Icterus jamacaii), and 183 122 Cacicus, and Psarocolius—as then defined, were not monophyletic. three members of the grackles and allies subfamily (Dives atrovio- 184 123 Lanyon and Omland (1999) found that Icteridae comprises five laceus, Curaeus forbesi, Macroagelaius subalaris).
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