Polyphyly of the hawk genera Leucopternis and Buteogallus (Aves, Accipitridae): multiple habitat shifts during the Neotropical buteonine diversification

Abstract Background The family Accipitridae (hawks, eagles and Old World vultures) represents a large radiation of predatory birds with an almost global distribution, although most species of this family occur in the Neotropics. Despite great morphological and ecological diversity, the evolutionary relationships in the family have been poorly explored at all taxonomic levels. Using sequences from four mitochondrial genes (12S, ATP8, ATP6, and ND6), we reconstructed the phylogeny of the Neotropical forest hawk genus Leucopternis and most of the allied genera of Neotropical buteonines. Our goals were to infer the evolutionary relationships among species of Leucopternis, estimate their relationships to other buteonine genera, evaluate the phylogenetic significance of the white and black plumage patterns common to most Leucopternis species, and assess general patterns of diversification of the group with respect to species' affiliations with Neotropical regions and habitats. Results Our molecular phylogeny for the genus Leucopternis and its allies disagrees sharply with traditional taxonomic arrangements for the group, and we present new hypotheses of relationships for a number of species. The mtDNA phylogenetic trees derived from analysis of the combined data posit a polyphyletic relationship among species of Leucopternis, Buteogallus and Buteo. Three highly supported clades containing Leucopternis species were recovered in our phylogenetic reconstructions. The first clade consisted of the sister pairs L. lacernulatus and Buteogallus meridionalis, and Buteogallus urubitinga and Harpyhaliaetus coronatus, in addition to L. schistaceus and L. plumbeus. The second clade included the sister pair Leucopternis albicollis and L. occidentalis as well as L. polionotus. The third lineage comprised the sister pair L. melanops and L. kuhli, in addition to L. semiplumbeus and Buteo buteo. According to our results, the white and black plumage patterns have evolved at least twice in the group. Furthermore, species found to the east and west of the Andes (cis-Andean and trans-Andean, respectively) are not reciprocally monophyletic, nor are forest and non-forest species. Conclusion The polyphyly of Leucopternis, Buteogallus and Buteo establishes a lack of concordance of current Accipitridae taxonomy with the mtDNA phylogeny for the group, and points to the need for further phylogenetic analysis at all taxonomic levels in the family as also suggested by other recent analyses. Habitat shifts, as well as cis- and trans-Andean disjunctions, took place more than once during buteonine diversification in the Neotropical region. Overemphasis of the black and white plumage patterns has led to questionable conclusions regarding the relationships of Leucopternis species, and suggests more generally that plumage characters should be used with considerable caution in the taxonomic evaluation of the Accipitridae.

We thank the following individuals and institutions for kindly providing samples, without which this work could not have been performed: Donna Dittman, Robb Brumfield and Fred Sheldon (LSUMZ); Leo Joseph (ANSP); Alexandre Aleixo and Marcos Pérsio D. Santos (MPEG); Marcelo Soares (UFPA); Carlos E. A. Carvalho; Eduardo P. M. de Carvalho Filho; Giancarlo Zorzin, Gustavo D. M. de Carvalho and Marcus Canuto (SOS Falconiformes), Pedro Scherer Neto (Museu de História Natural Capão do Imbuía), Zoológico de Paulínia, Ricardo Pereira (Zoológico de São Paulo), Leo Fukui and Jorge Lisboa (ABPFAR); David Whitacre, Rick Watson and Martin Gilbert (Peregrine Fund); Tammo Hoeksema (ZOOMAT); Sérgio Aguilar (Veracruz Pronatura); Alexandre Miranda, José H. Fontenele, Greicelene R. Pedro (Orquidário de Santos); Renato Gaban-Lima and Guilherme Renzo (USP); Adriana Joppert (DEPAVE/SP); Robson Silva e Silva and Fábio Olmos. We are grateful to Erika S. Tavares for kindly sequencing the ANSP samples at the Royal Ontario Museum and helping with the analyses, and Allan Baker for allowing use of the ROM laboratory for sequencing. We also thank Sérgio Pereira and Martin Riesing for useful suggestions and support, Erwin T. Grau for invaluable help with the laboratory methods, Robb Brumfield for help with the analyses, and Camila Ribas, Cibele Biondo, Gustavo S. Cabanne, Rodrigo Pessoa and three anonymous referees for comments and several contributions to the manuscript. Financial support was provided by Fundação de Amparo a Pesquisa do Estado de São Paulo, CNPq and CAPES.

We thank the following individuals and institutions for kindly providing samples, without which this work could not have been performed: Donna Dittman, Robb Brumfield and Fred Sheldon (LSUMZ); Leo Joseph (ANSP); Alexandre Aleixo and Marcos Pérsio D. Santos (MPEG); Marcelo Soares (UFPA); Carlos E. A. Carvalho; Eduardo P. M. de Carvalho Filho; Giancarlo Zorzin, Gustavo D. M. de Carvalho and Marcus Canuto (SOS Falconiformes), Pedro Scherer Neto (Museu de História Natural Capão do Imbuía), Zoológico de Paulínia, Ricardo Pereira (Zoológico de São Paulo), Leo Fukui and Jorge Lisboa (ABPFAR); David Whitacre, Rick Watson and Martin Gilbert (Peregrine Fund); Tammo Hoeksema (ZOOMAT); Sérgio Aguilar (Veracruz Pronatura); Alexandre Miranda, José H. Fontenele, Greicelene R. Pedro (Orquidário de Santos); Renato GabanLima and Guilherme Renzo (USP); Adriana Joppert (DEPAVE/SP); Robson Silva e Silva and Fábio Olmos. We are grateful to Erika S. Tavares for kindly sequencing the ANSP samples at the Royal Ontario Museum and helping with the analyses, and Allan Baker for allowing use of the ROM laboratory for sequencing. We also thank Sérgio Pereira and Martin Riesing for useful suggestions and support, Erwin T. Grau for invaluable help with the laboratory methods, Robb Brumfield for help with the analyses, and Camila Ribas, Cibele Biondo, Gustavo S. Cabanne, Rodrigo Pessoa and three anonymous referees for comments and several contributions to the manuscript. Financial support was provided by Fundação de Amparo a Pesquisa do Estado de São Paulo, CNPq and CAPES.