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      Whole-genome analyses resolve early branches in the tree of life of modern birds.

      1 , 2 , 3 , 4 , 5 , 6 , 7 , 8 , 9 , 10 , 11 , 11 , 12 , 13 , 13 , 13 , 13 , 14 , 15 , 10 , 16 , 2 , 10 , 17 , 18 , 19 , 19 , 20 , 21 , 21 , 12 , 22 , 23 , 24 , 25 , 26 , 27 , 28 , 29 , 29 , 30 , 31 , 32 , 32 , 33 , 34 , 34 , 35 , 36 , 12 , 12 , 12 , 12 , 37 , 37 , 38 , 39 , 40 ,   41 , 17 , 42 , 43 , 44 , 24 , 13 , 13 , 13 , 13 , 13 , 13 , 13 , 13 , 13 , 13 , 45 , 45 , 11 , 46 , 47 , 48 , 12 , 49 , 50 , 51 , 52 , 53 , 54 , 55 , 56 ,   12 , 57 , 58 , 59 , 60 , 11 , 61 , 62 , 63 , 64 , 65 , 66 , 67 , 68 , 69 , 70
      Science (New York, N.Y.)
      American Association for the Advancement of Science (AAAS)

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          Abstract

          To better determine the history of modern birds, we performed a genome-scale phylogenetic analysis of 48 species representing all orders of Neoaves using phylogenomic methods created to handle genome-scale data. We recovered a highly resolved tree that confirms previously controversial sister or close relationships. We identified the first divergence in Neoaves, two groups we named Passerea and Columbea, representing independent lineages of diverse and convergently evolved land and water bird species. Among Passerea, we infer the common ancestor of core landbirds to have been an apex predator and confirm independent gains of vocal learning. Among Columbea, we identify pigeons and flamingoes as belonging to sister clades. Even with whole genomes, some of the earliest branches in Neoaves proved challenging to resolve, which was best explained by massive protein-coding sequence convergence and high levels of incomplete lineage sorting that occurred during a rapid radiation after the Cretaceous-Paleogene mass extinction event about 66 million years ago.

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          Most cited references138

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          Identification of common molecular subsequences.

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            Comparison of phylogenetic trees

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              BIONJ: an improved version of the NJ algorithm based on a simple model of sequence data.

              O. Gascuel (1997)
              We propose an improved version of the neighbor-joining (NJ) algorithm of Saitou and Nei. This new algorithm, BIONJ, follows the same agglomerative scheme as NJ, which consists of iteratively picking a pair of taxa, creating a new mode which represents the cluster of these taxa, and reducing the distance matrix by replacing both taxa by this node. Moreover, BIONJ uses a simple first-order model of the variances and covariances of evolutionary distance estimates. This model is well adapted when these estimates are obtained from aligned sequences. At each step it permits the selection, from the class of admissible reductions, of the reduction which minimizes the variance of the new distance matrix. In this way, we obtain better estimates to choose the pair of taxa to be agglomerated during the next steps. Moreover, in comparison with NJ's estimates, these estimates become better and better as the algorithm proceeds. BIONJ retains the good properties of NJ--especially its low run time. Computer simulations have been performed with 12-taxon model trees to determine BIONJ's efficiency. When the substitution rates are low (maximum pairwise divergence approximately 0.1 substitutions per site) or when they are constant among lineages, BIONJ is only slightly better than NJ. When the substitution rates are higher and vary among lineages,BIONJ clearly has better topological accuracy. In the latter case, for the model trees and the conditions of evolution tested, the topological error reduction is on the average around 20%. With highly-varying-rate trees and with high substitution rates (maximum pairwise divergence approximately 1.0 substitutions per site), the error reduction may even rise above 50%, while the probability of finding the correct tree may be augmented by as much as 15%.
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                Author and article information

                Journal
                Science
                Science (New York, N.Y.)
                American Association for the Advancement of Science (AAAS)
                1095-9203
                0036-8075
                Dec 12 2014
                : 346
                : 6215
                Affiliations
                [1 ] Department of Neurobiology, Howard Hughes Medical Institute (HHMI), and Duke University Medical Center, Durham, NC 27710, USA. jarvis@neuro.duke.edu tandywarnow@gmail.com mtpgilbert@gmail.com wangj@genomics.cn zhanggj@genomics.cn.
                [2 ] Department of Computer Science, The University of Texas at Austin, Austin, TX 78712, USA.
                [3 ] Scientific Computing Group, Heidelberg Institute for Theoretical Studies, Heidelberg, Germany.
                [4 ] China National GeneBank, BGI-Shenzhen, Shenzhen 518083, China. College of Medicine and Forensics, Xi'an Jiaotong University Xi'an 710061, China. Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Øster Voldgade 5-7, 1350 Copenhagen, Denmark.
                [5 ] Department of Biology, New Mexico State University, Las Cruces, NM 88003, USA.
                [6 ] China National GeneBank, BGI-Shenzhen, Shenzhen 518083, China. Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Øster Voldgade 5-7, 1350 Copenhagen, Denmark.
                [7 ] School of Biological Sciences, University of Sydney, Sydney, New South Wales 2006, Australia.
                [8 ] Department of Ecology and Evolutionary Biology, University of California, Los Angeles, CA 90095, USA. Department of Biological Sciences, Louisiana State University, Baton Rouge, LA 70803, USA.
                [9 ] CNRS UMR 5554, Institut des Sciences de l'Evolution de Montpellier, Université Montpellier II Montpellier, France.
                [10 ] Department of Neurobiology, Howard Hughes Medical Institute (HHMI), and Duke University Medical Center, Durham, NC 27710, USA.
                [11 ] Department of Evolutionary Biology, Evolutionary Biology Centre, Uppsala University, SE-752 36 Uppsala Sweden.
                [12 ] Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Øster Voldgade 5-7, 1350 Copenhagen, Denmark.
                [13 ] China National GeneBank, BGI-Shenzhen, Shenzhen 518083, China.
                [14 ] Department of Biology, New Mexico State University, Las Cruces, NM 88003, USA. Biodiversity and Biocomplexity Unit, Okinawa Institute of Science and Technology Onna-son, Okinawa 904-0495, Japan.
                [15 ] Department of Statistics and Institute of Bioinformatics, University of Georgia, Athens, GA 30602, USA.
                [16 ] Laboratoire de Biométrie et Biologie Evolutive, Centre National de la Recherche Scientifique, Université de Lyon, F-69622 Villeurbanne, France.
                [17 ] Environmental Futures Research Institute, Griffith University, Nathan, Queensland 4111, Australia.
                [18 ] Bioinformatics and Genomics Programme, Centre for Genomic Regulation, Dr. Aiguader 88, 08003 Barcelona, Spain. Universitat Pompeu Fabra, Barcelona, Spain. Institució Catalana de Recerca i Estudis Avançats, Barcelona, Spain.
                [19 ] Bioinformatics and Genomics Programme, Centre for Genomic Regulation, Dr. Aiguader 88, 08003 Barcelona, Spain. Universitat Pompeu Fabra, Barcelona, Spain.
                [20 ] Joint Institute for Computational Sciences, The University of Tennessee, Oak Ridge National Laboratory, Oak Ridge, TN 37831, USA.
                [21 ] Bioinformatics Research Centre, Aarhus University, DK-8000 Aarhus C, Denmark.
                [22 ] The Genome Institute, Washington University School of Medicine, St Louis, MI 63108, USA.
                [23 ] Department of Biochemistry, Molecular Biology, Entomology and Plant Pathology, Mississippi State University, Mississippi State, MS 39762, USA. Institute for Genomics, Biocomputing and Biotechnology, Mississippi State University, Mississippi State, MS 39762, USA. Department of Biological Sciences, Texas Tech University, Lubbock, TX 79409, USA.
                [24 ] Department of Ecology and Evolutionary Biology, University of California Santa Cruz (UCSC), Santa Cruz, CA 95064, USA.
                [25 ] Organisms and Environment Division, Cardiff School of Biosciences, Cardiff University Cardiff CF10 3AX, Wales, UK.
                [26 ] Organisms and Environment Division, Cardiff School of Biosciences, Cardiff University Cardiff CF10 3AX, Wales, UK. Key Laboratory of Animal Ecology and Conservation Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China.
                [27 ] International Wildlife Consultants, Carmarthen SA33 5YL, Wales, UK.
                [28 ] College of Medicine and Forensics, Xi'an Jiaotong University Xi'an, 710061, China.
                [29 ] State Key Laboratory for Agrobiotechnology, China Agricultural University, Beijing 100094, China.
                [30 ] Department of Ecology and Evolutionary Biology, Tulane University, New Orleans, LA 70118, USA. Museum of Natural Science and Department of Biological Sciences, Louisiana State University, Baton Rouge, LA 70803, USA.
                [31 ] Center for Zoo and Wild Animal Health, Copenhagen Zoo Roskildevej 38, DK-2000 Frederiksberg, Denmark.
                [32 ] Museum of Natural Science and Department of Biological Sciences, Louisiana State University, Baton Rouge, LA 70803, USA.
                [33 ] Department of Behavioral Neuroscience, Oregon Health and Science University, Portland, OR 97239, USA. Brazilian Avian Genome Consortium (CNPq/FAPESPA-SISBIO Aves), Federal University of Para, Belem, Para, Brazil.
                [34 ] Department of Behavioral Neuroscience, Oregon Health and Science University, Portland, OR 97239, USA.
                [35 ] Brazilian Avian Genome Consortium (CNPq/FAPESPA-SISBIO Aves), Federal University of Para, Belem, Para, Brazil. Institute of Biological Sciences, Federal University of Para, Belem, Para, Brazil.
                [36 ] Brazilian Avian Genome Consortium (CNPq/FAPESPA-SISBIO Aves), Federal University of Para, Belem, Para, Brazil. Institute of Medical Biochemistry Leopoldo de Meis, Federal University of Rio de Janeiro, Rio de Janeiro RJ 21941-902, Brazil.
                [37 ] Centre for Biological Sequence Analysis, Department of Systems Biology, Technical University of Denmark Kemitorvet 208, 2800 Kgs Lyngby, Denmark.
                [38 ] Breeding Centre for Endangered Arabian Wildlife, Sharjah, United Arab Emirates.
                [39 ] Dubai Falcon Hospital, Dubai, United Arab Emirates.
                [40 ] Canterbury Museum Rolleston Avenue, Christchurch 8050, New Zealand.
                [41 ] Trace and Environmental DNA Laboratory Department of Environment and Agriculture, Curtin University, Perth, Western Australia 6102, Australia.
                [42 ] Department of Integrative Biology, University of California, Berkeley, CA 94720, USA.
                [43 ] Laboratory of Genomic Diversity, National Cancer Institute Frederick, MD 21702, USA. Institute of Molecular and Cellular Biology, SB RAS and Novosibirsk State University, Novosibirsk, Russia.
                [44 ] Smithsonian Institution National Museum of Natural History, Washington, DC 20013, USA.
                [45 ] BGI-Shenzhen, Shenzhen 518083, China.
                [46 ] Department of Biological Sciences, National University of Singapore, Republic of Singapore.
                [47 ] Department of Vertebrate Zoology, National Museum of Natural History, Smithsonian Suitland, MD 20746, USA.
                [48 ] Center for Macroecology, Evolution and Climate, Natural History Museum of Denmark, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen Ø, Denmark.
                [49 ] Bell Museum of Natural History, University of Minnesota, Saint Paul, MN 55108, USA.
                [50 ] Center for Macroecology, Evolution and Climate, Natural History Museum of Denmark, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen Ø, Denmark. Department of Life Sciences, Natural History Museum, Cromwell Road, London SW7 5BD, UK. Department of Life Sciences, Imperial College London, Silwood Park Campus, Ascot SL5 7PY, UK.
                [51 ] Smithsonian Conservation Biology Institute, National Zoological Park, Front Royal, VA 22630, USA.
                [52 ] Smithsonian Conservation Biology Institute, National Zoological Park, Washington, DC 20008, USA.
                [53 ] Theodosius Dobzhansky Center for Genome Bioinformatics, St. Petersburg State University, St. Petersburg, Russia 199004. Oceanographic Center, Nova Southeastern University, Ft Lauderdale, FL 33004, USA.
                [54 ] Center for Biomolecular Science and Engineering, UCSC, Santa Cruz, CA 95064, USA.
                [55 ] San Diego Zoo Institute for Conservation Research, Escondido, CA 92027, USA.
                [56 ] Center for Macroecology, Evolution and Climate, Natural History Museum of Denmark, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen Ø, Denmark. Department of Life Sciences, Imperial College London, Silwood Park Campus, Ascot SL5 7PY, UK.
                [57 ] Center for Macroecology, Evolution and Climate, Natural History Museum of Denmark, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen Ø, Denmark. Department of Vertebrate Zoology, MRC-116, National Museum of Natural History, Smithsonian Institution, Washington, DC 20013, USA.
                [58 ] Department of Environmental Health Science, University of Georgia, Athens, GA 30602, USA.
                [59 ] Moore Laboratory of Zoology and Department of Biology, Occidental College, Los Angeles, CA 90041, USA.
                [60 ] Department of Genomics and Genetics, The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush Campus, Midlothian EH25 9RG, UK.
                [61 ] Swedish Species Information Centre, Swedish University of Agricultural Sciences Box 7007, SE-750 07 Uppsala, Sweden. Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China.
                [62 ] Department of Organismic and Evolutionary Biology and Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138, USA.
                [63 ] Scientific Computing Group, Heidelberg Institute for Theoretical Studies, Heidelberg, Germany. Institute of Theoretical Informatics, Department of Informatics, Karlsruhe Institute of Technology, D- 76131 Karlsruhe, Germany.
                [64 ] Department of Biochemistry and Biophysics, University of California, San Francisco, CA 94158, USA.
                [65 ] Department of Ornithology, American Museum of Natural History, New York, NY 10024, USA.
                [66 ] Department of Biology and Genetics Institute, University of Florida, Gainesville, FL 32611, USA.
                [67 ] Department of Computer Science, The University of Texas at Austin, Austin, TX 78712, USA. Departments of Bioengineering and Computer Science, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA. jarvis@neuro.duke.edu tandywarnow@gmail.com mtpgilbert@gmail.com wangj@genomics.cn zhanggj@genomics.cn.
                [68 ] BGI-Shenzhen, Shenzhen 518083, China. Department of Biology, University of Copenhagen, Ole Maaløes Vej 5, 2200 Copenhagen, Denmark. Princess Al Jawhara Center of Excellence in the Research of Hereditary Disorders, King Abdulaziz University, Jeddah 21589, Saudi Arabia. Macau University of Science and Technology, Avenida Wai long, Taipa, Macau 999078, China. Department of Medicine, University of Hong Kong, Hong Kong. jarvis@neuro.duke.edu tandywarnow@gmail.com mtpgilbert@gmail.com wangj@genomics.cn zhanggj@genomics.cn.
                [69 ] Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Øster Voldgade 5-7, 1350 Copenhagen, Denmark. Trace and Environmental DNA Laboratory Department of Environment and Agriculture, Curtin University, Perth, Western Australia 6102, Australia. jarvis@neuro.duke.edu tandywarnow@gmail.com mtpgilbert@gmail.com wangj@genomics.cn zhanggj@genomics.cn.
                [70 ] China National GeneBank, BGI-Shenzhen, Shenzhen 518083, China. Centre for Social Evolution, Department of Biology, Universitetsparken 15, University of Copenhagen, DK-2100 Copenhagen, Denmark. jarvis@neuro.duke.edu tandywarnow@gmail.com mtpgilbert@gmail.com wangj@genomics.cn zhanggj@genomics.cn.
                Article
                346/6215/1320 NIHMS678366
                10.1126/science.1253451
                4405904
                25504713
                2bc78633-9f1e-487e-8b57-0eb53b65ce3f
                History

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