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

Author:

Jarvis Erich D.1,Mirarab Siavash2,Aberer Andre J.3,Li Bo456,Houde Peter7,Li Cai46,Ho Simon Y. W.8,Faircloth Brant C.910,Nabholz Benoit11,Howard Jason T.1,Suh Alexander12,Weber Claudia C.12,da Fonseca Rute R.6,Li Jianwen4,Zhang Fang4,Li Hui4,Zhou Long4,Narula Nitish713,Liu Liang14,Ganapathy Ganesh1,Boussau Bastien15,Bayzid Md. Shamsuzzoha2,Zavidovych Volodymyr1,Subramanian Sankar16,Gabaldón Toni171819,Capella-Gutiérrez Salvador1718,Huerta-Cepas Jaime1718,Rekepalli Bhanu20,Munch Kasper21,Schierup Mikkel21,Lindow Bent6,Warren Wesley C.22,Ray David232425,Green Richard E.26,Bruford Michael W.27,Zhan Xiangjiang2728,Dixon Andrew29,Li Shengbin30,Li Ning31,Huang Yinhua31,Derryberry Elizabeth P.3233,Bertelsen Mads Frost34,Sheldon Frederick H.33,Brumfield Robb T.33,Mello Claudio V.3536,Lovell Peter V.35,Wirthlin Morgan35,Schneider Maria Paula Cruz3637,Prosdocimi Francisco3638,Samaniego José Alfredo6,Velazquez Amhed Missael Vargas6,Alfaro-Núñez Alonzo6,Campos Paula F.6,Petersen Bent39,Sicheritz-Ponten Thomas39,Pas An40,Bailey Tom41,Scofield Paul42,Bunce Michael43,Lambert David M.16,Zhou Qi44,Perelman Polina4546,Driskell Amy C.47,Shapiro Beth26,Xiong Zijun4,Zeng Yongli4,Liu Shiping4,Li Zhenyu4,Liu Binghang4,Wu Kui4,Xiao Jin4,Yinqi Xiong4,Zheng Qiuemei4,Zhang Yong4,Yang Huanming48,Wang Jian48,Smeds Linnea12,Rheindt Frank E.49,Braun Michael50,Fjeldsa Jon51,Orlando Ludovic6,Barker F. Keith52,Jønsson Knud Andreas515354,Johnson Warren55,Koepfli Klaus-Peter56,O’Brien Stephen5758,Haussler David59,Ryder Oliver A.60,Rahbek Carsten5154,Willerslev Eske6,Graves Gary R.5161,Glenn Travis C.62,McCormack John63,Burt Dave64,Ellegren Hans12,Alström Per6566,Edwards Scott V.67,Stamatakis Alexandros368,Mindell David P.69,Cracraft Joel70,Braun Edward L.71,Warnow Tandy272,Jun Wang4873747576,Gilbert M. Thomas P.643,Zhang Guojie477

Affiliation:

1. Department of Neurobiology, Howard Hughes Medical Institute (HHMI), and Duke University Medical Center, Durham, NC 27710, USA.

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.

5. College of Medicine and Forensics, Xi’an Jiaotong University Xi’an 710061, China.

6. Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Øster Voldgade 5-7, 1350 Copenhagen, Denmark.

7. Department of Biology, New Mexico State University, Las Cruces, NM 88003, USA.

8. School of Biological Sciences, University of Sydney, Sydney, New South Wales 2006, Australia.

9. Department of Ecology and Evolutionary Biology, University of California, Los Angeles, CA 90095, USA.

10. Department of Biological Sciences, Louisiana State University, Baton Rouge, LA 70803, USA.

11. CNRS UMR 5554, Institut des Sciences de l’Evolution de Montpellier, Université Montpellier II Montpellier, France.

12. Department of Evolutionary Biology, Evolutionary Biology Centre, Uppsala University, SE-752 36 Uppsala Sweden.

13. Biodiversity and Biocomplexity Unit, Okinawa Institute of Science and Technology Onna-son, Okinawa 904-0495, Japan.

14. Department of Statistics and Institute of Bioinformatics, University of Georgia, Athens, GA 30602, USA.

15. Laboratoire de Biométrie et Biologie Evolutive, Centre National de la Recherche Scientifique, Université de Lyon, F-69622 Villeurbanne, France.

16. Environmental Futures Research Institute, Griffith University, Nathan, Queensland 4111, Australia.

17. Bioinformatics and Genomics Programme, Centre for Genomic Regulation, Dr. Aiguader 88, 08003 Barcelona, Spain.

18. Universitat Pompeu Fabra, Barcelona, Spain.

19. Institució Catalana de Recerca i Estudis Avançats, 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.

24. Institute for Genomics, Biocomputing and Biotechnology, Mississippi State University, Mississippi State, MS 39762, USA.

25. Department of Biological Sciences, Texas Tech University, Lubbock, TX 79409, USA.

26. Department of Ecology and Evolutionary Biology, University of California Santa Cruz (UCSC), Santa Cruz, CA 95064, USA.

27. Organisms and Environment Division, Cardiff School of Biosciences, Cardiff University Cardiff CF10 3AX, Wales, UK.

28. Key Laboratory of Animal Ecology and Conservation Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China.

29. International Wildlife Consultants, Carmarthen SA33 5YL, Wales, UK.

30. College of Medicine and Forensics, Xi’an Jiaotong University Xi’an, 710061, China.

31. State Key Laboratory for Agrobiotechnology, China Agricultural University, Beijing 100094, China.

32. Department of Ecology and Evolutionary Biology, Tulane University, New Orleans, LA 70118, USA.

33. Museum of Natural Science and Department of Biological Sciences, Louisiana State University, Baton Rouge, LA 70803, USA.

34. Center for Zoo and Wild Animal Health, Copenhagen Zoo Roskildevej 38, DK-2000 Frederiksberg, Denmark.

35. Department of Behavioral Neuroscience, Oregon Health and Science University, Portland, OR 97239, USA.

36. Brazilian Avian Genome Consortium (CNPq/FAPESPA-SISBIO Aves), Federal University of Para, Belem, Para, Brazil.

37. Institute of Biological Sciences, Federal University of Para, Belem, Para, Brazil.

38. Institute of Medical Biochemistry Leopoldo de Meis, Federal University of Rio de Janeiro, Rio de Janeiro RJ 21941-902, Brazil.

39. Centre for Biological Sequence Analysis, Department of Systems Biology, Technical University of Denmark Kemitorvet 208, 2800 Kgs Lyngby, Denmark.

40. Breeding Centre for Endangered Arabian Wildlife, Sharjah, United Arab Emirates.

41. Dubai Falcon Hospital, Dubai, United Arab Emirates.

42. Canterbury Museum Rolleston Avenue, Christchurch 8050, New Zealand.

43. Trace and Environmental DNA Laboratory Department of Environment and Agriculture, Curtin University, Perth, Western Australia 6102, Australia.

44. Department of Integrative Biology, University of California, Berkeley, CA 94720, USA.

45. Laboratory of Genomic Diversity, National Cancer Institute Frederick, MD 21702, USA.

46. Institute of Molecular and Cellular Biology, SB RAS and Novosibirsk State University, Novosibirsk, Russia.

47. Smithsonian Institution National Museum of Natural History, Washington, DC 20013, USA.

48. BGI-Shenzhen, Shenzhen 518083, China.

49. Department of Biological Sciences, National University of Singapore, Republic of Singapore.

50. Department of Vertebrate Zoology, National Museum of Natural History, Smithsonian Suitland, MD 20746, USA.

51. Center for Macroecology, Evolution and Climate, Natural History Museum of Denmark, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen Ø, Denmark.

52. Bell Museum of Natural History, University of Minnesota, Saint Paul, MN 55108, USA.

53. Department of Life Sciences, Natural History Museum, Cromwell Road, London SW7 5BD, UK.

54. Department of Life Sciences, Imperial College London, Silwood Park Campus, Ascot SL5 7PY, UK.

55. Smithsonian Conservation Biology Institute, National Zoological Park, Front Royal, VA 22630, USA.

56. Smithsonian Conservation Biology Institute, National Zoological Park, Washington, DC 20008, USA.

57. Theodosius Dobzhansky Center for Genome Bioinformatics, St. Petersburg State University, St. Petersburg, Russia 199004.

58. Oceanographic Center, Nova Southeastern University, Ft Lauderdale, FL 33004, USA.

59. Center for Biomolecular Science and Engineering, UCSC, Santa Cruz, CA 95064, USA.

60. San Diego Zoo Institute for Conservation Research, Escondido, CA 92027, USA.

61. Department of Vertebrate Zoology, MRC-116, National Museum of Natural History, Smithsonian Institution, Washington, DC 20013, USA.

62. Department of Environmental Health Science, University of Georgia, Athens, GA 30602, USA.

63. Moore Laboratory of Zoology and Department of Biology, Occidental College, Los Angeles, CA 90041, USA.

64. 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.

65. Swedish Species Information Centre, Swedish University of Agricultural Sciences Box 7007, SE-750 07 Uppsala, Sweden.

66. Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China.

67. Department of Organismic and Evolutionary Biology and Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138, USA.

68. Institute of Theoretical Informatics, Department of Informatics, Karlsruhe Institute of Technology, D- 76131 Karlsruhe, Germany.

69. Department of Biochemistry and Biophysics, University of California, San Francisco, CA 94158, USA.

70. Department of Ornithology, American Museum of Natural History, New York, NY 10024, USA.

71. Department of Biology and Genetics Institute, University of Florida, Gainesville, FL 32611, USA.

72. Departments of Bioengineering and Computer Science, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA.

73. Department of Biology, University of Copenhagen, Ole Maaløes Vej 5, 2200 Copenhagen, Denmark.

74. Princess Al Jawhara Center of Excellence in the Research of Hereditary Disorders, King Abdulaziz University, Jeddah 21589, Saudi Arabia.

75. Macau University of Science and Technology, Avenida Wai long, Taipa, Macau 999078, China.

76. Department of Medicine, University of Hong Kong, Hong Kong.

77. Centre for Social Evolution, Department of Biology, Universitetsparken 15, University of Copenhagen, DK-2100 Copenhagen, Denmark.

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.

Publisher

American Association for the Advancement of Science (AAAS)

Subject

Multidisciplinary

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