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Science
Vol. 346 no. 6215 pp. 1320-1331
DOI: 10.1126/science.1253451
  • Research Article

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

  1. Guojie Zhang4,77,
  1. 1Department of Neurobiology, Howard Hughes Medical Institute (HHMI), and Duke University Medical Center, Durham, NC 27710, USA.
  2. 2Department of Computer Science, The University of Texas at Austin, Austin, TX 78712, USA.
  3. 3Scientific Computing Group, Heidelberg Institute for Theoretical Studies, Heidelberg, Germany.
  4. 4China National GeneBank, BGI-Shenzhen, Shenzhen 518083, China.
  5. 5College of Medicine and Forensics, Xi’an Jiaotong University Xi’an 710061, China.
  6. 6Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Øster Voldgade 5-7, 1350 Copenhagen, Denmark.
  7. 7Department of Biology, New Mexico State University, Las Cruces, NM 88003, USA.
  8. 8School of Biological Sciences, University of Sydney, Sydney, New South Wales 2006, Australia.
  9. 9Department of Ecology and Evolutionary Biology, University of California, Los Angeles, CA 90095, USA.
  10. 10Department of Biological Sciences, Louisiana State University, Baton Rouge, LA 70803, USA.
  11. 11CNRS UMR 5554, Institut des Sciences de l’Evolution de Montpellier, Université Montpellier II Montpellier, France.
  12. 12Department of Evolutionary Biology, Evolutionary Biology Centre, Uppsala University, SE-752 36 Uppsala Sweden.
  13. 13Biodiversity and Biocomplexity Unit, Okinawa Institute of Science and Technology Onna-son, Okinawa 904-0495, Japan.
  14. 14Department of Statistics and Institute of Bioinformatics, University of Georgia, Athens, GA 30602, USA.
  15. 15Laboratoire de Biométrie et Biologie Evolutive, Centre National de la Recherche Scientifique, Université de Lyon, F-69622 Villeurbanne, France.
  16. 16Environmental Futures Research Institute, Griffith University, Nathan, Queensland 4111, Australia.
  17. 17Bioinformatics and Genomics Programme, Centre for Genomic Regulation, Dr. Aiguader 88, 08003 Barcelona, Spain.
  18. 18Universitat Pompeu Fabra, Barcelona, Spain.
  19. 19Institució Catalana de Recerca i Estudis Avançats, Barcelona, Spain.
  20. 20Joint Institute for Computational Sciences, The University of Tennessee, Oak Ridge National Laboratory, Oak Ridge, TN 37831, USA.
  21. 21Bioinformatics Research Centre, Aarhus University, DK-8000 Aarhus C, Denmark.
  22. 22The Genome Institute, Washington University School of Medicine, St Louis, MI 63108, USA.
  23. 23Department of Biochemistry, Molecular Biology, Entomology and Plant Pathology, Mississippi State University, Mississippi State, MS 39762, USA.
  24. 24Institute for Genomics, Biocomputing and Biotechnology, Mississippi State University, Mississippi State, MS 39762, USA.
  25. 25Department of Biological Sciences, Texas Tech University, Lubbock, TX 79409, USA.
  26. 26Department of Ecology and Evolutionary Biology, University of California Santa Cruz (UCSC), Santa Cruz, CA 95064, USA.
  27. 27Organisms and Environment Division, Cardiff School of Biosciences, Cardiff University Cardiff CF10 3AX, Wales, UK.
  28. 28Key Laboratory of Animal Ecology and Conservation Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China.
  29. 29International Wildlife Consultants, Carmarthen SA33 5YL, Wales, UK.
  30. 30College of Medicine and Forensics, Xi’an Jiaotong University Xi’an, 710061, China.
  31. 31State Key Laboratory for Agrobiotechnology, China Agricultural University, Beijing 100094, China.
  32. 32Department of Ecology and Evolutionary Biology, Tulane University, New Orleans, LA 70118, USA.
  33. 33Museum of Natural Science and Department of Biological Sciences, Louisiana State University, Baton Rouge, LA 70803, USA.
  34. 34Center for Zoo and Wild Animal Health, Copenhagen Zoo Roskildevej 38, DK-2000 Frederiksberg, Denmark.
  35. 35Department of Behavioral Neuroscience, Oregon Health and Science University, Portland, OR 97239, USA.
  36. 36Brazilian Avian Genome Consortium (CNPq/FAPESPA-SISBIO Aves), Federal University of Para, Belem, Para, Brazil.
  37. 37Institute of Biological Sciences, Federal University of Para, Belem, Para, Brazil.
  38. 38Institute of Medical Biochemistry Leopoldo de Meis, Federal University of Rio de Janeiro, Rio de Janeiro RJ 21941-902, Brazil.
  39. 39Centre for Biological Sequence Analysis, Department of Systems Biology, Technical University of Denmark Kemitorvet 208, 2800 Kgs Lyngby, Denmark.
  40. 40Breeding Centre for Endangered Arabian Wildlife, Sharjah, United Arab Emirates.
  41. 41Dubai Falcon Hospital, Dubai, United Arab Emirates.
  42. 42Canterbury Museum Rolleston Avenue, Christchurch 8050, New Zealand.
  43. 43Trace and Environmental DNA Laboratory Department of Environment and Agriculture, Curtin University, Perth, Western Australia 6102, Australia.
  44. 44Department of Integrative Biology, University of California, Berkeley, CA 94720, USA.
  45. 45Laboratory of Genomic Diversity, National Cancer Institute Frederick, MD 21702, USA.
  46. 46Institute of Molecular and Cellular Biology, SB RAS and Novosibirsk State University, Novosibirsk, Russia.
  47. 47Smithsonian Institution National Museum of Natural History, Washington, DC 20013, USA.
  48. 48BGI-Shenzhen, Shenzhen 518083, China.
  49. 49Department of Biological Sciences, National University of Singapore, Republic of Singapore.
  50. 50Department of Vertebrate Zoology, National Museum of Natural History, Smithsonian Suitland, MD 20746, USA.
  51. 51Center for Macroecology, Evolution and Climate, Natural History Museum of Denmark, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen Ø, Denmark.
  52. 52Bell Museum of Natural History, University of Minnesota, Saint Paul, MN 55108, USA.
  53. 53Department of Life Sciences, Natural History Museum, Cromwell Road, London SW7 5BD, UK.
  54. 54Department of Life Sciences, Imperial College London, Silwood Park Campus, Ascot SL5 7PY, UK.
  55. 55Smithsonian Conservation Biology Institute, National Zoological Park, Front Royal, VA 22630, USA.
  56. 56Smithsonian Conservation Biology Institute, National Zoological Park, Washington, DC 20008, USA.
  57. 57Theodosius Dobzhansky Center for Genome Bioinformatics, St. Petersburg State University, St. Petersburg, Russia 199004.
  58. 58Oceanographic Center, Nova Southeastern University, Ft Lauderdale, FL 33004, USA.
  59. 59Center for Biomolecular Science and Engineering, UCSC, Santa Cruz, CA 95064, USA.
  60. 60San Diego Zoo Institute for Conservation Research, Escondido, CA 92027, USA.
  61. 61Department of Vertebrate Zoology, MRC-116, National Museum of Natural History, Smithsonian Institution, Washington, DC 20013, USA.
  62. 62Department of Environmental Health Science, University of Georgia, Athens, GA 30602, USA.
  63. 63Moore Laboratory of Zoology and Department of Biology, Occidental College, Los Angeles, CA 90041, USA.
  64. 64Department of Genomics and Genetics, The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush Campus, Midlothian EH25 9RG, UK.
  65. 65Swedish Species Information Centre, Swedish University of Agricultural Sciences Box 7007, SE-750 07 Uppsala, Sweden.
  66. 66Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China.
  67. 67Department of Organismic and Evolutionary Biology and Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138, USA.
  68. 68Institute of Theoretical Informatics, Department of Informatics, Karlsruhe Institute of Technology, D- 76131 Karlsruhe, Germany.
  69. 69Department of Biochemistry and Biophysics, University of California, San Francisco, CA 94158, USA.
  70. 70Department of Ornithology, American Museum of Natural History, New York, NY 10024, USA.
  71. 71Department of Biology and Genetics Institute, University of Florida, Gainesville, FL 32611, USA.
  72. 72Departments of Bioengineering and Computer Science, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA.
  73. 73Department of Biology, University of Copenhagen, Ole Maaløes Vej 5, 2200 Copenhagen, Denmark.
  74. 74Princess Al Jawhara Center of Excellence in the Research of Hereditary Disorders, King Abdulaziz University, Jeddah 21589, Saudi Arabia.
  75. 75Macau University of Science and Technology, Avenida Wai long, Taipa, Macau 999078, China.
  76. 76Department of Medicine, University of Hong Kong, Hong Kong.
  77. 77Centre for Social Evolution, Department of Biology, Universitetsparken 15, University of Copenhagen, DK-2100 Copenhagen, Denmark.
  1. †Corresponding author. E-mail: jarvis{at}neuro.duke.edu (E.D.J.); tandywarnow{at}gmail.com (T.W.); mtpgilbert{at}gmail.com (M.T.P.G.); wangj{at}genomics.cn (W.J.); zhanggj{at}genomics.cn (G. Z.)
  1. * These authors contributed equally to this work.

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.

  • Received for publication 17 March 2014.
  • Accepted for publication 15 October 2014.