Comparative genomics reveals insights into avian genome evolution and adaptation

Author:

Zhang Guojie12,Li Cai13,Li Qiye13,Li Bo1,Larkin Denis M.4,Lee Chul56,Storz Jay F.7,Antunes Agostinho89,Greenwold Matthew J.10,Meredith Robert W.11,Ödeen Anders12,Cui Jie1314,Zhou Qi15,Xu Luohao116,Pan Hailin1,Wang Zongji117,Jin Lijun1,Zhang Pei1,Hu Haofu1,Yang Wei1,Hu Jiang1,Xiao Jin1,Yang Zhikai1,Liu Yang1,Xie Qiaolin1,Yu Hao1,Lian Jinmin1,Wen Ping1,Zhang Fang1,Li Hui1,Zeng Yongli1,Xiong Zijun1,Liu Shiping117,Zhou Long1,Huang Zhiyong1,An Na1,Wang Jie118,Zheng Qiumei1,Xiong Yingqi1,Wang Guangbiao1,Wang Bo1,Wang Jingjing1,Fan Yu19,da Fonseca Rute R.3,Alfaro-Núñez Alonzo3,Schubert Mikkel3,Orlando Ludovic3,Mourier Tobias3,Howard Jason T.20,Ganapathy Ganeshkumar20,Pfenning Andreas20,Whitney Osceola20,Rivas Miriam V.20,Hara Erina20,Smith Julia20,Farré Marta4,Narayan Jitendra21,Slavov Gancho21,Romanov Michael N22,Borges Rui89,Machado João Paulo823,Khan Imran89,Springer Mark S.24,Gatesy John24,Hoffmann Federico G.2526,Opazo Juan C.27,Håstad Olle28,Sawyer Roger H.10,Kim Heebal5629,Kim Kyu-Won5,Kim Hyeon Jeong6,Cho Seoae6,Li Ning30,Huang Yinhua3031,Bruford Michael W.32,Zhan Xiangjiang3233,Dixon Andrew34,Bertelsen Mads F.35,Derryberry Elizabeth3637,Warren Wesley38,Wilson Richard K38,Li Shengbin39,Ray David A.26,Green Richard E.40,O’Brien Stephen J.4142,Griffin Darren22,Johnson Warren E.43,Haussler David40,Ryder Oliver A.44,Willerslev Eske3,Graves Gary R.4546,Alström Per4748,Fjeldså Jon46,Mindell David P.49,Edwards Scott V.50,Braun Edward L.51,Rahbek Carsten4652,Burt David W.53,Houde Peter54,Zhang Yong1,Yang Huanming155,Wang Jian1,Jarvis Erich D.20,Gilbert M. Thomas P.356,Wang Jun155575859,Ye Chen,Liang Shaoguang,Yan Zengli,Zepeda M. Lisandra,Campos Paula F.,Velazquez Amhed Missael Vargas,Samaniego José Alfredo,Avila-Arcos María,Martin Michael D.,Barnett Ross,Ribeiro Angela M.,Mello Claudio V.,Lovell Peter V.,Almeida Daniela,Maldonado Emanuel,Pereira Joana,Sunagar Kartik,Philip Siby,Dominguez-Bello Maria Gloria,Bunce Michael,Lambert David,Brumfield Robb T.,Sheldon Frederick H.,Holmes Edward C.,Gardner Paul P.,Steeves Tammy E.,Stadler Peter F.,Burge Sarah W.,Lyons Eric,Smith Jacqueline,McCarthy Fiona,Pitel Frederique,Rhoads Douglas,Froman David P.,

Affiliation:

1. China National GeneBank, Beijing Genomics Institute (BGI)–Shenzhen, Shenzhen, 518083, China.

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

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

4. Royal Veterinary College, University of London, London, UK.

5. Interdisciplinary Program in Bioinformatics, Seoul National University, Seoul 151-742, Republic of Korea.

6. Cho and Kim Genomics, Seoul National University Research Park, Seoul 151-919, Republic of Korea.

7. School of Biological Sciences, University of Nebraska, Lincoln, NE 68588, USA.

8. Centro de Investigación en Ciencias del Mar y Limnología (CIMAR)/Centro Interdisciplinar de Investigação Marinha e Ambiental (CIIMAR), Universidade do Porto, Rua dos Bragas, 177, 4050-123 Porto, Portugal.

9. Departamento de Biologia, Faculdade de Ciências, Universidade do Porto, Rua do Campo Alegre, 4169-007 Porto, Portugal.

10. Department of Biological Sciences, University of South Carolina, Columbia, SC, USA.

11. Department of Biology and Molecular Biology, Montclair State University, Montclair, NJ 07043, USA.

12. Department of Animal Ecology, Uppsala University, Norbyvägen 18D, S-752 36 Uppsala, Sweden.

13. Marie Bashir Institute for Infectious Diseases and Biosecurity, Charles Perkins Centre, School of Biological Sciences and Sydney Medical School, The University of Sydney, Sydney, NSW 2006, Australia.

14. Program in Emerging Infectious Diseases, Duke-NUS Graduate Medical School, Singapore 169857, Singapore.

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

16. College of Life Sciences, Wuhan University, Wuhan 430072, China.

17. School of Bioscience and Bioengineering, South China University of Technology, Guangzhou 510006, China.

18. BGI Education Center,University of Chinese Academy of Sciences,Shenzhen, 518083, China.

19. Key Laboratory of Animal Models and Human Disease Mechanisms of Chinese Academy of Sciences and Yunnan Province, Kunming Institute of Zoology, Kunming, Yunnan 650223, China.

20. Department of Neurobiology, Howard Hughes Medical Institute, Duke University Medical Center, Durham, NC 27710, USA.

21. Institute of Biological, Environmental and Rural Sciences, Aberystwyth University, Aberystwyth, UK.

22. School of Biosciences, University of Kent, Canterbury CT2 7NJ, UK.

23. Instituto de Ciências Biomédicas Abel Salazar (ICBAS), Universidade do Porto, Portugal.

24. Department of Biology, University of California Riverside, Riverside, CA 92521, USA.

25. Department of Biochemistry, Molecular Biology, Entomology and Plant Pathology, Mississippi State University, Mississippi State, MS 39762, USA.

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

27. Instituto de Ciencias Ambientales y Evolutivas, Facultad de Ciencias, Universidad Austral de Chile, Valdivia, Chile.

28. Department of Anatomy, Physiology and Biochemistry, Swedish University of Agricultural Sciences, Post Office Box 7011, S-750 07, Uppsala, Sweden.

29. Department of Agricultural Biotechnology and Research Institute for Agriculture and Life Sciences, Seoul National University, Seoul 151-742, Republic of Korea.

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

31. College of Animal Science and Technology, China Agricultural University, Beijing 100094, China.

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

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

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

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

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

37. Museum of Natural Science, Louisiana State University, Baton Rouge, LA 70803, USA.

38. The Genome Institute at Washington University, St. Louis, MO 63108, USA.

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

40. Department of Biomolecular Engineering, University of California, Santa Cruz, CA 95064, USA.

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

42. Nova Southeastern University Oceanographic Center 8000 N Ocean Drive, Dania, FL 33004, USA.

43. Smithsonian Conservation Biology Institute, National Zoological Park, 1500 Remount Road, Front Royal, VA 22630, USA.

44. Genetics Division, San Diego Zoo Institute for Conservation Research, 15600 San Pasqual Valley Road, Escondido, CA 92027, USA.

45. Department of Vertebrate Zoology, MRC-116, National Museum of Natural History, Smithsonian Institution, Post Office Box 37012, Washington, DC 20013-7012, USA.

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

47. Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, 1 Beichen West Road, Chaoyang District, Beijing 100101, China.

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

49. Department of Biochemistry & Biophysics, University of California, San Francisco, CA 94158, USA.

50. Department of Organismic and Evolutionary Biology and Museum of Comparative Zoology, Harvard University, 26 Oxford Street, Cambridge, MA 02138, USA.

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

52. Imperial College London, Grand Challenges in Ecosystems and the Environment Initiative, Silwood Park Campus, Ascot, Berkshire SL5 7PY, UK.

53. Division of Genetics and Genomics, The Roslin Institute and Royal (Dick) School of Veterinary Studies, The Roslin Institute Building, University of Edinburgh, Easter Bush Campus, Midlothian EH25 9RG, UK.

54. Department of Biology, New Mexico State University, Box 30001 MSC 3AF, Las Cruces, NM 88003, USA.

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

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

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

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

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

Abstract

Birds are the most species-rich class of tetrapod vertebrates and have wide relevance across many research fields. We explored bird macroevolution using full genomes from 48 avian species representing all major extant clades. The avian genome is principally characterized by its constrained size, which predominantly arose because of lineage-specific erosion of repetitive elements, large segmental deletions, and gene loss. Avian genomes furthermore show a remarkably high degree of evolutionary stasis at the levels of nucleotide sequence, gene synteny, and chromosomal structure. Despite this pattern of conservation, we detected many non-neutral evolutionary changes in protein-coding genes and noncoding regions. These analyses reveal that pan-avian genomic diversity covaries with adaptations to different lifestyles and convergent evolution of traits.

Publisher

American Association for the Advancement of Science (AAAS)

Subject

Multidisciplinary

Reference192 articles.

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