Molecular Phylogenetics and Evolution 77 (2014) 177–182
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Molecular Phylogenetics and Evolution
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Short Communication A comprehensive multilocus assessment of sparrow (Aves: Passerellidae) relationships ⇑ John Klicka a, , F. Keith Barker b,c, Kevin J. Burns d, Scott M. Lanyon b, Irby J. Lovette e, Jaime A. Chaves f,g, Robert W. Bryson Jr. a a Department of Biology and Burke Museum of Natural History and Culture, University of Washington, Box 353010, Seattle, WA 98195-3010, USA b Department of Ecology, Evolution, and Behavior, University of Minnesota, 100 Ecology Building, 1987 Upper Buford Circle, St. Paul, MN 55108, USA c Bell Museum of Natural History, University of Minnesota, 100 Ecology Building, 1987 Upper Buford Circle, St. Paul, MN 55108, USA d Department of Biology, San Diego State University, San Diego, CA 92182, USA e Fuller Evolutionary Biology Program, Cornell Lab of Ornithology, Cornell University, 159 Sapsucker Woods Road, Ithaca, NY 14950, USA f Department of Biology, University of Miami, 1301 Memorial Drive, Coral Gables, FL 33146, USA g Universidad San Francisco de Quito, USFQ, Colegio de Ciencias Biológicas y Ambientales, y Extensión Galápagos, Campus Cumbayá, Casilla Postal 17-1200-841, Quito, Ecuador article info abstract
Article history: The New World sparrows (Emberizidae) are among the best known of songbird groups and have long- Received 6 November 2013 been recognized as one of the prominent components of the New World nine-primaried oscine assem- Revised 16 April 2014 blage. Despite receiving much attention from taxonomists over the years, and only recently using molec- Accepted 21 April 2014 ular methods, was a ‘‘core’’ sparrow clade established allowing the reconstruction of a phylogenetic Available online 30 April 2014 hypothesis that includes the full sampling of sparrow species diversity. In this paper, we use mitochon- drial DNA gene sequences from all 129 putative species of sparrow and four additional (nuclear) loci for a Keywords: subset of these taxa to resolve both generic and species level relationships. Hypotheses derived from our Nine-primaried oscine families mitochondrial (2184 base pairs) and nuclear (5705 base pairs) DNA data sets were generally in agree- Passerellidae Sparrow taxonomy ment with respect to clade constituency but differed somewhat with respect to among-clade relation- Systematics ships. Sparrow diversity is defined predominantly by eight well-supported clades that indicate a lack of monophyly for at least three currently recognized genera. Ammodramus is polyphyletic and requires the naming of two additional genera. Spizella is also polyphyletic with Tree Sparrow (Spizella arborea) as a taxonomic ‘‘outlier’’. Pselliophorus is embedded within a larger Atlapetes assemblage and should be merged with that group. This new hypothesis of sparrow relationships will form the basis for future com- parative analyses of variation within songbirds. Ó 2014 Elsevier Inc. All rights reserved.
1. Introduction included all nine-primaried oscine genera (Barker et al., 2013). In this work, sparrows (Passerellidae) are recognized as one of five Within the New World nine-primaried oscine assemblage, feed- ‘‘core’’ lineages within this radiation. They are now placed apart ing specializations have historically been used as a guideline for from the Old World radiation of buntings (Emberiza and allies) that assigning membership to groups. Among finch-billed birds, the retains the former sparrow family name, Emberizidae. This defini- ‘‘sparrows and buntings’’ have long been considered a ‘‘natural tive list of Passerellidae members now includes 129 species orga- group’’ and have been recognized variously as a tribe (Emberizini; nized into 25 genera. Sibley and Monroe, 1990), subfamily (Emberizinae; e.g. AOU, 1931, Previous molecular studies have focused mostly on particular 1957), or family (Emberizidae; AOU, 1998). Constituency in this clades within the Passerellidae. For example, phylogenetic rela- group has been further refined as molecular phylogenies have tionships within the genera Pipilo and Aimophila (DaCosta et al., become available (e.g. Sibley and Ahlquist, 1990; Klicka et al., 2009), Spizella (e.g. Dodge et al., 1995), Ammodrammus (Zink and 2000; Yuri and Mindell, 2002), and only recently has a definitive Avise, 1990), Zonotrichia (Zink and Blackwell, 1996), and Melospiza list of members emerged based on a broad multilocus study that (Zink and Blackwell, op. cit.) have all been recently explored. Phy- logenies derived in these works not only inform taxonomic deci- sions, but also provide the evolutionary context necessary to ⇑ Corresponding author. understand the evolution of morphological traits, historical E-mail address: [email protected] (J. Klicka). http://dx.doi.org/10.1016/j.ympev.2014.04.025 1055-7903/Ó 2014 Elsevier Inc. All rights reserved. 178 J. Klicka et al. / Molecular Phylogenetics and Evolution 77 (2014) 177–182 biogeography, and the processes that lead to speciation. At the selected were GTR + I + G (cyt-b, ND2, FGB-I5, RAG-1), GTR + G family level (i.e. all of Passerellidae), such investigations are ham- (ACO1), and HKY + G (MYO-I2). We then used maximum-likeli- pered because a comprehensive phylogenetic hypothesis has not hood (RAxML v7.0.3; Stamatakis, 2006) and Bayesian (MrBayes yet been constructed. The goal of this study is to provide such a v3.1.2; Ronquist and Huelsenbeck, 2003) methods to estimate phy- treatment for the entire sparrow radiation by using complete spe- logenetic trees for the larger (128 putative sparrow species, 152 cies-level sampling and a set of both mitochondrial (mtDNA) and species overall) mtDNA data set. The data were partitioned by nuclear (nucDNA) sequence markers. gene. For the ML analysis, we used the GTRGAMMA model and per- formed 1000 nonparametric rapid bootstrap replicates to assess nodal support. We used only Bayesian inference for the reduced 2. Methods mtDNA and nucDNA data sets (n = 82 taxa). For the Bayesian anal- ysis, we performed at least two independent runs from random 2.1. Taxon sampling and lab protocols starting trees, each for 3 million generations, with trees and parameters sampled every 100 generations. We applied a 25% We gathered 129 individuals representing each putative spar- burn-in after checking for convergence using TRACER v1.4 row species from among the 25 genera (Appendix A, Table S1) (Rambaut and Drummond, 2007) and AWTY (Nylander et al., recently identified as comprising the newly defined sparrow family 2008) to confirm that the standard deviation of split frequencies Passerellidae (Barker et al., 2013). Importantly, a number of taxa approached zero. The resulting trees were used to calculate poster- traditionally recognized as sparrows are not a part of this new ior probabilities in a 50% majority-rule consensus tree. We arrangement including Calcarius and Plectrophenax (now in Calcar- repeated the Bayesian analysis for the reduced mtDNA and concat- iidae), Emberiza and allies (now sole occupants of the former spar- enated nuDNA data sets (n = 82 taxa) and for each nuclear gene. row family, Emberizidae, sensu Barker et al., 2013), and a suite of We also reconstructed a species tree from both the mtDNA and finch-billed birds, now collectively referred to as tanager-finches nuDNA loci using ⁄BEAST (Heled and Drummond, 2010), a part of (see for example Sibley and Ahlquist, 1990; Burns et al., 2002; the BEAST v1.6.2 package (Drummond and Rambaut, 2007). We Klicka et al., 2007; Barker et al., 2013; these taxa are now in Thra- linked the two mtDNA genes, which represent a single locus, in a upidae). Conversely, two genera formerly considered members of single tree but unlinked substitution and clock models. Trees and Thraupidae but now known to belong within Passerellidae, Chloro- substitution and clock models were unlinked for the nuclear genes. spingus and Oreothraupis, were included. We chose as outgroups We used a Yule speciation prior and relaxed uncorrelated lognor- single representatives of genera from the songbird families most mal clock for each gene tree. Two independent analyses were con- closely related to sparrows (Klicka et al., 2000), warblers (Paruli- ducted with 250 million generations and sampling every 7500 dae, n = 9) and blackbirds (Icteridae, n = 13; see Table S1 for com- generations. Convergence between these runs and appropriate plete listing). A more distantly related tanager (Thraupidae; burn-in was assessed by examining ESS values and likelihood plots Saltator aurantiirostris) was used to root the entire assemblage. in TRACER. We extracted total genomic DNA using a DNeasy tissue extrac- tion kit (Qiagen, Valencia, CA) following the manufacturer’s proto- col. We sequenced the mitochondrial DNA genes cytochrome b 3. Results (cyt-b, 1143 base pairs, bp) and NADH dehydrogenase subunit 2 (ND2, 1041 bp) using methods previously described (Klicka and 3.1. Phylogenetic reconstruction Spellman, 2007). DNA was extracted from toepads for nine taxa (Table S1) not yet represented in frozen tissue collections. For The full mtDNA data set contained 321 parsimony-informative these, one or more fragments of cyt-b (only) were amplified in a sites (cyt-b: 469 in 1143 bp; ND2: 548/1041). The nuclear gene loci lab where avian molecular work had not previously been con- contained less variation than the mtDNA genes (parsimony-infor- ducted (see Klicka and Spellman, 2007 for protocol). mative sites: ACO1, 232/1305; MYO-I2, 83/887; FGB-I5, 98/614; For a subset of specimens (n=82, 74 sparrows and 8 outgroup RAG-1, 235/2899). taxa), we also sequenced four nuclear introns, including 1305 bp of Both ML and Bayesian analyses of the completely sampled aconitase 1 intron 9 (ACO1), 887 bp of myoglobin intron 2 (MYO- (mtDNA) data set yielded similar topologies (Fig. 1) that had no I2), 614 bp of beta-fibrinogen intron 5 (FGB-I5), and 2899 bp of well-supported nodes in conflict. A single taxon, the narrowly dis- recombination activating gene 1 (RAG-1), using primers identified tributed west Andean endemic, Chlorospingus flavovirens, fell out- by Kimball et al. (2009) and Groth and Barrowclough (1999). side the sparrow assemblage and within the tanagers Amplifications were done in 12.5 lL reactions under the following (Thraupidae). With a couple of exceptions (Pezopetes capitalis, Tor- conditions: denaturation at 94 °C, followed by 35 cycles of 94 °C for reornis inexpectata), the remaining 128 sparrow taxa were orga- 30 s, 60 °C for 45 s, and 72 °C for 1 min. This was followed by a nized into eight major clades (Fig. 1, A–H) discussed below. The 10 min extension at 72 °C. PCR products were sent to the High- topology shown (Fig. 1) represents our ‘‘best estimate’’ (sensu Throughput Genomics Unit (HGTU, University of Washington) for Lanyon, 1993) of relationships within sparrows and is the first pub- sequencing. We edited and manually aligned forward and reverse lished hypothesis of sparrow relationships that is comprehensive sequences for each individual using Sequencher v4.2 (Gene Codes in scope. Corporation, Ann Arbor, MI). Heterozygous sites in nuclear loci Bayesian analyses performed on the abridged mtDNA (Fig. 2a) were coded with the appropriate IUPAC ambiguity code. All and concatenated nucDNA (Fig. 2b) data sets recovered the same sequences were deposited in GenBank (accession numbers XXX– eight core clades. Relationships within each of these clades were XXX). relatively stable across analyses, although the mtDNA and nucDNA trees suggested slightly differing arrangements among these 2.2. Phylogenetic analysis clades. The former placed clades G (Arremonops and allies) and H (Chlorospingus, see Fig. 2) in a polytomy at the base of the tree Before proceeding with phylogenetic analyses, we determined and a sister relationship between the more derived clades A the best-fit model of evolution for each mitochondrial and nuclear (Melospiza and allies) and B + C; (Melozone-Atlapetes-Pipilo and gene with jModeltest v0.1.0. (Posada, 2008) using the Akaike Infor- allies), whereas the latter suggested that clade F (Spizella and allies) mation Criterion (AIC, Burnham and Anderson, 2002). The models was sister to the rest of the sparrows, and clades A and D J. Klicka et al. / Molecular Phylogenetics and Evolution 77 (2014) 177–182 179
Fig. 1. Phylogeny of the avian family Passerellidae inferred from mitochondrial DNA sequence data. Best maximum likelihood tree shown, and numbers at nodes indicate support values (maximum likelihood bootstrap followed by Bayesian posterior probability). Nodes supported by less than 70% bootstrap or 50% Bayesian posterior probability denoted by dashes (–). Capital letters A–H identify the eight main individual sparrow clades that are discussed in the text. This tree represents our ‘‘best’’ estimate of phylogenetic relationships within the Passerellidae. 180 J. Klicka et al. / Molecular Phylogenetics and Evolution 77 (2014) 177–182
Fig. 2. Bayesian estimates of phylogeny for a subset of sparrow taxa of the avian family Passerellidae. (a) gene tree based on partitioned mtDNA only, (b) gene tree based on concatenated nucDNA only, and (c) species tree based on both mtDNA and nuDNA loci. Color-coded clades correspond with clades A–H as defined earlier (see Fig. 1). Only strongly supported nodes (P70% bootstrap support and P95% Bayesian posterior probability) that were retained across all analyses shown.
(Zonotrichia-Junco and allies) were sister, exclusive of B + C. Indi- the monotypic Mexican endemics Xenospiza and Oriturus. These vidual gene trees were generally poorly resolved but contained are mostly members of traditionally recognized North American many of the same eight core clades (Appendix A, Fig. S1). Our ‘‘grassland’’ and ‘‘brushland’’ sparrow assemblages (e.g. Paynter, reconstructed species tree using all loci (Fig. 2c) provided no sup- 1964; Dickerman et al., 1967; Robins and Schnell, 1971). Relation- port either way for the mtDNA or nucDNA relationships. In fact, all ships within this clade have previously been discussed (Klicka and conflicting nodes received low posterior probability support in the Spellman, 2007) and taxonomic recommendations suggested. ⁄BEAST phylogeny and yielded a five-way polytomy at the base of Among these, a single taxonomic issue exists that remains to be the tree. This species tree represents our most ‘‘reliable estimate’’ addressed. Ammodramus is polyphyletic, with elements split (sensu Lanyon, 1993) of sparrow relationships. Clearly, the four among subclades within this clade and others placed distantly nuclear markers and single mtDNA markers used were not suffi- within the sparrow tree (clade G). The type species for this genus cient to completely disentangle questions of sparrow relationships (savannarum, see A. bimaculatus; Swainson, 1837) is among those and additional work on this group is warranted. more distantly placed, necessitating that new names be given to those forms occupying the present clade. We suggest that Ammosp- iza (Oberholser, 1905) be resurrected for the leconteii-maritimus- 4. Discussion nelsoni-caudacutus clade and Passserherbulus (Stone 1907) for bair- dii-henslowi. As a more conservative alternative, bairdii-henslowi 4.1. Molecular systematics and taxonomy of the Passerellidae may be placed into a more inclusive new genus that includes all additional elements of the subclade (Passerculus, Melospiza, and Given philosophical differences among taxonomists regarding Xenospiza). From among these genera, Passerculus (Bonaparte generic level classification, it is difficult to make taxonomic recom- 1838) has priority and would be most appropriate. mendations that have broad appeal. Some view a taxonomy as a reflection of evolutionary pattern with the preference of ‘‘lumping’’ closely related taxa so that the nomenclature would more closely 4.1.2. Clade B + C, Melozone, Atlapetes, Pipilo and allies reflect or indicate relationships (e.g. Lovette et al., 2010). Others Clades B and C were sister groups across all analyses. Collec- use genera as ‘‘bins’’ to denote or categorize morphologic dissimi- tively, these represent independent lower latitude (mostly Central larity, irrespective of genetic affinity (e.g. AOU, 1998). These differ- and South America) sparrow radiations. Although Melozone and ing views may lead to a lack of consensus. Keeping this dichotomy Aimophila have recently been reconfigured (see DaCosta et al., in mind, we discuss the taxonomic implications of our study of 2009; Chesser et al., 2010), our analyses suggest that Melozone Passerellidae below. may now be paraphyletic with respect to Aimophila, and may in fact not form a clade. More data are required to address this uncer- 4.1.1. Clade A: Melospiza and allies tainty. We note, however, that the merging of these two genera Clade A includes Melospiza, Passerculus, Artemisiospiza, a subset would solve this taxonomic problem. In this case, Aimophila of a polyphyletic Ammodramus, the monotypic form Poocetes, and (Swainson, 1837) would have priority and Melozone J. Klicka et al. / Molecular Phylogenetics and Evolution 77 (2014) 177–182 181
(Reichenbach, 1850) would be abandoned. Elsewhere, Pipilo and this clade is appropriate given long branches connecting most of Atlapetes appear to be sister taxa according to all analyses (Figs. 1 them. and 2). Atlapetes, as configured, is paraphyletic with respect to Psel- Clade G is another speciose clade of mainly lower-latitude taxa, liophorus, the latter of which appear to be narrowly distributed comprised of Peucaea, Arremonops, Ammodramus, and Rhynchosp- melanistic forms of Atlapetes. We suggest that a merging of Psellio- iza. This clade accommodates several recent taxonomic revisions phorus (Ridgway, 1898) into Atlapetes (Wagler, 1831, type species (Chesser et al., 2010; Remsen et al., 2013) with no additional A. pileatus) is warranted. Two poorly known monotypic genera changes required at this time (providing Ammodramus polyphyly are also clearly members of this (B + C) clade, both relatively is addressed, see clade A, above). ancient lineages with no close relatives. These are the Cuban ende- Finally, clade H represents two new genera of sparrows that his- mic Torreornis and Pezopetes, an obscure finch from the highlands torically were included within Thraupidae (tanagers; e.g. Ridgway, of Costa Rica and Western Panama. 1902; Hellmayer, 1936). Oreothraupis is an obscure, monotypic form restricted in distribution to the subtropical regions of western Colombia and Ecuador. Chlorospingus (excepting C. flavovirens)isa 4.1.3. Clade D, Zonotrichia – Junco, and allies more widely distributed (and more speciose) cloud forest specialist With the exception of Melospiza, (see clade A), this clade con- that occurs in the appropriate habitat throughout the mountainous tains all of the elements of the historically defined ‘‘brush-inhabit- regions of Central and South America. Only recently (Barker et al., ing’’ (Paynter, 1964) or ‘‘brushland-nesting’’ sparrows (Dickerman 2013) was the correct placement with the New World Sparrows et al., 1967). Due to a number of well-documented intergeneric (Passerellidae) confirmed for these genera. hybridization events (e.g. Dickerman, 1961; Short and Simon, 1965), these taxa (i.e. Passerella, Melospiza, Zonotrichia, and Junco) have long been considered closely related species. Passerella and 5. Conclusion Melospiza have previously been merged into Zonotrichia (Paynter, 1964) and some authors have merged all three of these into Junco Modern taxonomies need be altered to include the 128 species (Short and Simon, 1965). The ‘‘brushland-nesting’’ sparrows as shown in Fig. 1 as these represent all known extant species within they were originally conceived do not form a clade (Klicka and the avian family Passerellidae (Barker et al., 2013). Importantly, Spellman, 2007, and this study) as Melospiza lies well outside the this assemblage now includes the two traditionally thraupid gen- assemblage, and a single member of Spizella (arborea; Fringilla era Chlorospingus and Oreothraupis (although the former is poly- arborea of Wilson, 1810) is embedded within it (see also Carson phyletic, with C. flavovirens remaining placed among the and Spicer, 2003). This renders Spizella polyphyletic and in need tanagers). It no longer includes Emberiza and its allies (Urocynch- of a taxonomic revision. The name Spizella (S. pusilla, Bonaparte, ramus, Melophus, Latoucheornis, Miliaria), nor does it include any 1831) should be retained by the remaining members of the genus of the taxa currently recognized as ‘‘tanager finches’’ (see (see below), leaving arborea in need of a new generic designation. Remsen et al., 2013). The latter includes 15 genera (Volatinia, Our mtDNA trees (Figs. 1 and 2a) suggest a sister relationship with Sporophila, Oryzoborus, Melopyrrha, Tiaris, Loxipasser, Loxigilla, the monotypic form Passerella although branch lengths suggest Euneornis, Melanospiza, Pinaroloxias, Haplospiza, Acanthidops, long independent histories. This putative sister-group relationship Diglossa, Sicalis, Emberizoides) still recognized as sparrows in some is equivocal according to our analyses of nucDNA (Fig. 2b and c). current taxonomies (e.g. AOU, 1998). We therefore suggest that a new genus be erected to accommodate Given the subjective nature of higher-level taxonomy, we focus Spizella arborea. In contrast, despite apparent hybridization events, only on those recommended changes that would eliminate para- or all analyses indicate that Junco and Zonotrichia form closely related polyphyly within the group as it is currently configured. Ammod- but monophyletic sister genera. ramus is polyphyletic; it is our recommendation that Ammospiza The placement of Clade D within the overall sparrow phylogeny (Oberholser, 1905) be resurrected for the leconteii-maritimus-nel- represents one of the few instances where our mtDNA and nucDNA soni-caudacutus clade and Passerherbulus (Stone, 1907) for bairdii- phylogeny estimates differ significantly. Mitochondrial DNA (Figs. 1 henslowi. Pselliophorus (two species) is embedded within an other- and 2a) indicates that clade D is sister to a larger clade that wise monophyletic Atlapetes and should be subsumed within the includes subclades A, B, and C; whereas, the nucDNA (Fig. 2b) sug- latter genus. Spizella is also polyphyletic. The most efficient and gests a sister relationship between clades A (‘‘grassland’’ sparrows) appropriate solution to this problem is to erect a new genus for and D (‘‘brushland’’ sparrows). Resolving this discrepancy will Spizella arborea. likely require the analysis of additional loci. Acknowledgments 4.2. The base of the tree, Clades E – H We wish to thank the curators and collection managers at the According to our *BEAST species tree, the remaining four clades institutions that provided tissue samples critical for the comple- E–H form a polytomy at the base of the sparrow topology (Fig. 2c). tion of this study. These include F. Sheldon, R. Brumfield, and D. However, mtDNA and nucDNA gene trees suggest slightly differing Dittmann (Louisiana State University Museum of Natural Science); arrangements. Following recent AOU revisions (Chesser et al., A. Navarro and O. Rojas (Universidad Nacional Autónoma de Méx- 2012; Remsen et al., 2013), clade E is comprised of all members ico, Museo de Zoologia); N. Johnson and C. Cicero (University of of a single genus, Arremon, despite the fact that it contains multi- California, Berkeley, Museum of Vertebrate Zoology); R. Zink ple, deeply split subclades. For comparison, clade A contains a sim- (James Ford Bell Museum of Natural History); S. Hackett and J. ilar structure and number of taxa yet it is divided into no fewer Bates (Field Museum of Natural History); S. Rowher and S. Birks than seven unique genera. This contrast highlights the outcomes (University of Washington, Burke Museum of Natural History); of disparate taxonomic approaches (‘‘lumpers’’ vs ‘‘binners’’). A sis- M. Robbins and T. Peterson (University of Kansas Natural History ter relationship between Spizella and an Amphispiza-Chondestes- Museum); P. Escalante (Universidad Nacional Autónoma de Méxi- Calamospiza grouping occurs in clade F. This relationship was pre- co, Instituto de Biología, La Colección Nacional de Aves); D. Cadena viously suggested (with lower support) in earlier work with less (Universidad de los Andes, Instituto Alexander von Humboldt, and complete taxon sampling (Carson and Spicer, 2003; DaCosta Instituto de Ciencias Naturales – Universidad Nacional de Colom- et al., 2009). We suggest that retention of all of the genera within bia, Colección Zoológica de la Universidad del Tolima); 182 J. Klicka et al. / Molecular Phylogenetics and Evolution 77 (2014) 177–182
J. Pérez-Emán (Universidad Central de Venezuela, Instituto de Zoo- Heled, J., Drummond, A., 2010. Bayesian inference of species trees from multilocus logía y Ecología Tropical and Colección Ornitolólogia Phelps); S. data. Mol. Biol. Evol. 27, 570–580. Hellmayer, C.E., 1936. Catalogue of birds of the Americas. Field Museum Natural Edwards and J. Trimble (Museum of Comparative Zoology, Harvard History Publications, Zoological Series, vol. 13, pt. 9. University); and N. Rice (Academy of Natural Sciences of Drexel Kimball, R.T. et al., 2009. A well-tested set of primers to amplify regions spread University). A special thanks is due to the collectors, preparators, across the avian genome. Mol. Phylogenet. Evol. 50, 654–660. Klicka, J., Johnson, K.P., Lanyon, S.M., 2000. New World nine-primaried oscine and staffs who do much of the hard work behind the scenes at relationships: constructing mitochondrial DNA framework. Auk 117, 321–336. these institutions. Images used in the graphical abstract are Wiki- Klicka, J., Spellman, G., Burns, K., 2007. Defining a monophyletic Cardinalini: a media Commons files (S. arborea and J. hyemalis, author Simon molecular perspective. Mol. Phylogenet. Evol. 45, 1014–1032. Klicka, J., Spellman, G., 2007. A molecular evaluation of the North American Pierre Barrette; Z. leucophrys, author Wolfgang Wander). This work ‘‘Grassland’’ sparrow clade. Auk 124, 537–551. was funded in part by NSF DEB 0315469 (to JK), DEB-0315416 (to Lanyon, S.M., 1993. Phylogenetic frameworks: toward a firmer foundation for the KJB), DEB-0315218 (to IJL), and DEB-0316092 (to SML and FKB). comparative approach. Biol. J. Linn. Soc. 49, 45–61. Lovette, I.J., Péreez-Emán, J.L., Sullivan, J.P., Banks, R.C., Fiorentino, I., Córdoba- Córdoba, S., Echeverry-Galvis, M., Barker, F.K., Burns, K.J., Klicka, J., Lanyon, S.M., Appendix A. Supplementary material Bermingham, E., 2010. A comprehensive multilocus phylogeny for the wood- warblers and a revised classification of the Parulidae (Aves). Mole. Phylog. Evolution. 57, 753–770. Supplementary data associated with this article can be found, in Nylander, J.A., Wilgenbusch, J.C., Warren, D.L., Swofford, D.L., 2008. AWTY (are we the online version, at http://dx.doi.org/10.1016/j.ympev.2014.0 there yet): A system for graphicalexploration of MCMC convergence in Bayesian 4.025. phylogeneticinference. Bioinformatics 24, 581–583. Oberholser, H.C., 1905. Notes on the nomenclature of certain genera of birds. Smithsonian Miscell. Collect. 48, 59–68. References Paynter Jr., R.A., 1964. Generic limits of Zonotrichia. Condor 66, 277–281. Posada, D., 2008. JModelTest: phylogenetic model averaging. Mol. Biol. Evol. 25, American Ornithologists’ Union, 1931. Check-list of North American birds, fourth 1253–1256. ed., American Ornithologists’ Lancaster, PA. Rambaut, A., Drummond, A.J., 2007. Tracer v1.5. Available at: http:// American Ornithologists’ Union, 1957. Check-list of North American birds, fifth ed., beast.bio.ed.ac.uk/Tracer. American Ornithologists’ Union, Baltimore, MD. Reichenbach, L., 1850. Avium Systema Naturale. Das Natürlich System der Vögel. 36 American Ornithologists’ Union. 1998. Check-list of North American birds, seventh pp., plate 79. ed., American Ornithologists’ Union, Washington, DC. Remsen, J.V., Jr., Cadena, C.D., Jaramillo, A., Nores, M., Pacheco, J.F., Pérez-Emán, J., Barker, F.K., Burns, K.J., Klicka, J., Lanyon, S.M., Lovette, I.J., 2013. Going to extremes: Robbins, M.B., Stiles, F.G., Stotz, D.F., Zimmer, K.J., Version 30 August 2013. A contrasting rates of diversification in a recent radiation of New World Passerine classification of the bird species of South America. American Ornithologists’ birds. Syst. Biol. 62, 298–320. Union.