Comparative genomics reveals insights into avian genome evolution and adaptation

doi:10.1126/science.1251385

. 2014 Dec 12;346(6215):1311-20.

doi: 10.1126/science.1251385. Epub 2014 Dec 11.

Comparative genomics reveals insights into avian genome evolution and adaptation

Guojie Zhang¹, Cai Li², Qiye Li², Bo Li³, Denis M Larkin⁴, Chul Lee⁵, Jay F Storz⁶, Agostinho Antunes⁷, Matthew J Greenwold⁸, Robert W Meredith⁹, Anders Ödeen¹⁰, Jie Cui¹¹, Qi Zhou¹², Luohao Xu¹³, Hailin Pan³, Zongji Wang¹⁴, Lijun Jin³, Pei Zhang³, Haofu Hu³, Wei Yang³, Jiang Hu³, Jin Xiao³, Zhikai Yang³, Yang Liu³, Qiaolin Xie³, Hao Yu³, Jinmin Lian³, Ping Wen³, Fang Zhang³, Hui Li³, Yongli Zeng³, Zijun Xiong³, Shiping Liu¹⁴, Long Zhou³, Zhiyong Huang³, Na An³, Jie Wang¹⁵, Qiumei Zheng³, Yingqi Xiong³, Guangbiao Wang³, Bo Wang³, Jingjing Wang³, Yu Fan¹⁶, Rute R da Fonseca¹⁷, Alonzo Alfaro-Núñez¹⁷, Mikkel Schubert¹⁷, Ludovic Orlando¹⁷, Tobias Mourier¹⁷, Jason T Howard¹⁸, Ganeshkumar Ganapathy¹⁸, Andreas Pfenning¹⁸, Osceola Whitney¹⁸, Miriam V Rivas¹⁸, Erina Hara¹⁸, Julia Smith¹⁸, Marta Farré⁴, Jitendra Narayan¹⁹, Gancho Slavov¹⁹, Michael N Romanov²⁰, Rui Borges⁷, João Paulo Machado²¹, Imran Khan⁷, Mark S Springer²², John Gatesy²², Federico G Hoffmann²³, Juan C Opazo²⁴, Olle Håstad²⁵, Roger H Sawyer⁸, Heebal Kim²⁶, Kyu-Won Kim²⁷, Hyeon Jeong Kim²⁸, Seoae Cho²⁸, Ning Li²⁹, Yinhua Huang³⁰, Michael W Bruford³¹, Xiangjiang Zhan³², Andrew Dixon³³, Mads F Bertelsen³⁴, Elizabeth Derryberry³⁵, Wesley Warren³⁶, Richard K Wilson³⁶, Shengbin Li³⁷, David A Ray³⁸, Richard E Green³⁹, Stephen J O'Brien⁴⁰, Darren Griffin²⁰, Warren E Johnson⁴¹, David Haussler³⁹, Oliver A Ryder⁴², Eske Willerslev¹⁷, Gary R Graves⁴³, Per Alström⁴⁴, Jon Fjeldså⁴⁵, David P Mindell⁴⁶, Scott V Edwards⁴⁷, Edward L Braun⁴⁸, Carsten Rahbek⁴⁹, David W Burt⁵⁰, Peter Houde⁵¹, Yong Zhang³, Huanming Yang⁵², Jian Wang³; Avian Genome Consortium; Erich D Jarvis⁵³, M Thomas P Gilbert⁵⁴, Jun Wang⁵⁵

Collaborators, Affiliations

Collaborators

Affiliations

¹ China National GeneBank, Beijing Genomics Institute (BGI)-Shenzhen, Shenzhen, 518083, China. Centre for Social Evolution, Department of Biology, Universitetsparken 15, University of Copenhagen, DK-2100 Copenhagen, Denmark. zhanggj@genomics.cn jarvis@neuro.duke.edu mtpgilbert@gmail.com wangj@genomics.cn.
² China National GeneBank, Beijing Genomics Institute (BGI)-Shenzhen, Shenzhen, 518083, China. Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Øster Voldgade 5-7, 1350 Copenhagen, Denmark.
³ China National GeneBank, Beijing Genomics Institute (BGI)-Shenzhen, Shenzhen, 518083, China.
⁴ Royal Veterinary College, University of London, London, UK.
⁵ Interdisciplinary Program in Bioinformatics, Seoul National University, Seoul 151-742, Republic of Korea. Cho and Kim Genomics, Seoul National University Research Park, Seoul 151-919, Republic of Korea.
⁶ School of Biological Sciences, University of Nebraska, Lincoln, NE 68588, USA.
⁷ 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. Departamento de Biologia, Faculdade de Ciências, Universidade do Porto, Rua do Campo Alegre, 4169-007 Porto, Portugal.
⁸ Department of Biological Sciences, University of South Carolina, Columbia, SC, USA.
⁹ Department of Biology and Molecular Biology, Montclair State University, Montclair, NJ 07043, USA.
¹⁰ Department of Animal Ecology, Uppsala University, Norbyvägen 18D, S-752 36 Uppsala, Sweden.
¹¹ 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. Program in Emerging Infectious Diseases, Duke-NUS Graduate Medical School, Singapore 169857, Singapore.
¹² Department of Integrative Biology University of California, Berkeley, CA 94720, USA.
¹³ China National GeneBank, Beijing Genomics Institute (BGI)-Shenzhen, Shenzhen, 518083, China. College of Life Sciences, Wuhan University, Wuhan 430072, China.
¹⁴ China National GeneBank, Beijing Genomics Institute (BGI)-Shenzhen, Shenzhen, 518083, China. School of Bioscience and Bioengineering, South China University of Technology, Guangzhou 510006, China.
¹⁵ China National GeneBank, Beijing Genomics Institute (BGI)-Shenzhen, Shenzhen, 518083, China. BGI Education Center,University of Chinese Academy of Sciences,Shenzhen, 518083, China.
¹⁶ 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.
¹⁷ Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Øster Voldgade 5-7, 1350 Copenhagen, Denmark.
¹⁸ Department of Neurobiology, Howard Hughes Medical Institute, Duke University Medical Center, Durham, NC 27710, USA.
¹⁹ Institute of Biological, Environmental and Rural Sciences, Aberystwyth University, Aberystwyth, UK.
²⁰ School of Biosciences, University of Kent, Canterbury CT2 7NJ, UK.
²¹ 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. Instituto de Ciências Biomédicas Abel Salazar (ICBAS), Universidade do Porto, Portugal.
²² Department of Biology, University of California Riverside, Riverside, CA 92521, 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.
²⁴ Instituto de Ciencias Ambientales y Evolutivas, Facultad de Ciencias, Universidad Austral de Chile, Valdivia, Chile.
²⁵ Department of Anatomy, Physiology and Biochemistry, Swedish University of Agricultural Sciences, Post Office Box 7011, S-750 07, Uppsala, Sweden.
²⁶ Interdisciplinary Program in Bioinformatics, Seoul National University, Seoul 151-742, Republic of Korea. Cho and Kim Genomics, Seoul National University Research Park, Seoul 151-919, Republic of Korea. Department of Agricultural Biotechnology and Research Institute for Agriculture and Life Sciences, Seoul National University, Seoul 151-742, Republic of Korea.
²⁷ Interdisciplinary Program in Bioinformatics, Seoul National University, Seoul 151-742, Republic of Korea.
²⁸ Cho and Kim Genomics, Seoul National University Research Park, Seoul 151-919, Republic of Korea.
²⁹ State Key Laboratory for Agrobiotechnology, China Agricultural University, Beijing 100094, China.
³⁰ State Key Laboratory for Agrobiotechnology, China Agricultural University, Beijing 100094, China. College of Animal Science and Technology, China Agricultural University, Beijing 100094, China.
³¹ Organisms and Environment Division, Cardiff School of Biosciences, Cardiff University, Cardiff CF10 3AX, Wales, UK.
³² Organisms and Environment Division, Cardiff School of Biosciences, Cardiff University, Cardiff CF10 3AX, Wales, UK. Key Lab of Animal Ecology and Conservation Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101 China.
³³ International Wildlife Consultants, Carmarthen SA33 5YL, Wales, UK.
³⁴ Centre for Zoo and Wild Animal Health, Copenhagen Zoo, Roskildevej 38, DK-2000 Frederiksberg, Denmark.
³⁵ Department of Ecology and Evolutionary Biology, Tulane University, New Orleans, LA, USA. Museum of Natural Science, Louisiana State University, Baton Rouge, LA 70803, USA.
³⁶ The Genome Institute at Washington University, St. Louis, MO 63108, USA.
³⁷ College of Medicine and Forensics, Xi'an Jiaotong University, Xi'an, 710061, China.
³⁸ Institute for Genomics, Biocomputing and Biotechnology, Mississippi State University, Mississippi State, MS 39762, USA.
³⁹ Department of Biomolecular Engineering, University of California, Santa Cruz, CA 95064, USA.
⁴⁰ Theodosius Dobzhansky Center for Genome Bioinformatics, St. Petersburg State University, St. Petersburg, Russia. Nova Southeastern University Oceanographic Center 8000 N Ocean Drive, Dania, FL 33004, USA.
⁴¹ Smithsonian Conservation Biology Institute, National Zoological Park, 1500 Remount Road, Front Royal, VA 22630, USA.
⁴² Genetics Division, San Diego Zoo Institute for Conservation Research, 15600 San Pasqual Valley Road, Escondido, CA 92027, USA.
⁴³ Department of Vertebrate Zoology, MRC-116, National Museum of Natural History, Smithsonian Institution, Post Office Box 37012, Washington, DC 20013-7012, USA. Center for Macroecology, Evolution and Climate, the Natural History Museum of Denmark, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen O, Denmark.
⁴⁴ Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, 1 Beichen West Road, Chaoyang District, Beijing 100101, China. Swedish Species Information Centre, Swedish University of Agricultural Sciences, Box 7007, SE-750 07 Uppsala, Sweden.
⁴⁵ Center for Macroecology, Evolution and Climate, the Natural History Museum of Denmark, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen O, Denmark.
⁴⁶ Department of Biochemistry & Biophysics, University of California, San Francisco, CA 94158, USA.
⁴⁷ Department of Organismic and Evolutionary Biology and Museum of Comparative Zoology, Harvard University, 26 Oxford Street, Cambridge, MA 02138, USA.
⁴⁸ Department of Biology and Genetics Institute, University of Florida, Gainesville, FL 32611, USA.
⁴⁹ Center for Macroecology, Evolution and Climate, the Natural History Museum of Denmark, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen O, Denmark. Imperial College London, Grand Challenges in Ecosystems and the Environment Initiative, Silwood Park Campus, Ascot, Berkshire SL5 7PY, UK.
⁵⁰ 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.
⁵¹ Department of Biology, New Mexico State University, Box 30001 MSC 3AF, Las Cruces, NM 88003, USA.
⁵² China National GeneBank, Beijing Genomics Institute (BGI)-Shenzhen, Shenzhen, 518083, China. Macau University of Science and Technology, Avenida Wai long, Taipa, Macau 999078, China.
⁵³ Department of Neurobiology, Howard Hughes Medical Institute, Duke University Medical Center, Durham, NC 27710, USA. zhanggj@genomics.cn jarvis@neuro.duke.edu mtpgilbert@gmail.com wangj@genomics.cn.
⁵⁴ 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. zhanggj@genomics.cn jarvis@neuro.duke.edu mtpgilbert@gmail.com wangj@genomics.cn.
⁵⁵ China National GeneBank, Beijing Genomics Institute (BGI)-Shenzhen, Shenzhen, 518083, China. Macau University of Science and Technology, Avenida Wai long, Taipa, Macau 999078, 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. Department of Medicine, University of Hong Kong, Hong Kong. zhanggj@genomics.cn jarvis@neuro.duke.edu mtpgilbert@gmail.com wangj@genomics.cn.

PMID: 25504712
PMCID: PMC4390078
DOI: 10.1126/science.1251385

Comparative genomics reveals insights into avian genome evolution and adaptation

Guojie Zhang et al. Science. 2014.

. 2014 Dec 12;346(6215):1311-20.

doi: 10.1126/science.1251385. Epub 2014 Dec 11.

Authors

Collaborators

Affiliations

¹ China National GeneBank, Beijing Genomics Institute (BGI)-Shenzhen, Shenzhen, 518083, China. Centre for Social Evolution, Department of Biology, Universitetsparken 15, University of Copenhagen, DK-2100 Copenhagen, Denmark. zhanggj@genomics.cn jarvis@neuro.duke.edu mtpgilbert@gmail.com wangj@genomics.cn.
² China National GeneBank, Beijing Genomics Institute (BGI)-Shenzhen, Shenzhen, 518083, China. Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Øster Voldgade 5-7, 1350 Copenhagen, Denmark.
³ China National GeneBank, Beijing Genomics Institute (BGI)-Shenzhen, Shenzhen, 518083, China.
⁴ Royal Veterinary College, University of London, London, UK.
⁵ Interdisciplinary Program in Bioinformatics, Seoul National University, Seoul 151-742, Republic of Korea. Cho and Kim Genomics, Seoul National University Research Park, Seoul 151-919, Republic of Korea.
⁶ School of Biological Sciences, University of Nebraska, Lincoln, NE 68588, USA.
⁷ 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. Departamento de Biologia, Faculdade de Ciências, Universidade do Porto, Rua do Campo Alegre, 4169-007 Porto, Portugal.
⁸ Department of Biological Sciences, University of South Carolina, Columbia, SC, USA.
⁹ Department of Biology and Molecular Biology, Montclair State University, Montclair, NJ 07043, USA.
¹⁰ Department of Animal Ecology, Uppsala University, Norbyvägen 18D, S-752 36 Uppsala, Sweden.
¹¹ 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. Program in Emerging Infectious Diseases, Duke-NUS Graduate Medical School, Singapore 169857, Singapore.
¹² Department of Integrative Biology University of California, Berkeley, CA 94720, USA.
¹³ China National GeneBank, Beijing Genomics Institute (BGI)-Shenzhen, Shenzhen, 518083, China. College of Life Sciences, Wuhan University, Wuhan 430072, China.
¹⁴ China National GeneBank, Beijing Genomics Institute (BGI)-Shenzhen, Shenzhen, 518083, China. School of Bioscience and Bioengineering, South China University of Technology, Guangzhou 510006, China.
¹⁵ China National GeneBank, Beijing Genomics Institute (BGI)-Shenzhen, Shenzhen, 518083, China. BGI Education Center,University of Chinese Academy of Sciences,Shenzhen, 518083, China.
¹⁶ 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.
¹⁷ Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Øster Voldgade 5-7, 1350 Copenhagen, Denmark.
¹⁸ Department of Neurobiology, Howard Hughes Medical Institute, Duke University Medical Center, Durham, NC 27710, USA.
¹⁹ Institute of Biological, Environmental and Rural Sciences, Aberystwyth University, Aberystwyth, UK.
²⁰ School of Biosciences, University of Kent, Canterbury CT2 7NJ, UK.
²¹ 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. Instituto de Ciências Biomédicas Abel Salazar (ICBAS), Universidade do Porto, Portugal.
²² Department of Biology, University of California Riverside, Riverside, CA 92521, 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.
²⁴ Instituto de Ciencias Ambientales y Evolutivas, Facultad de Ciencias, Universidad Austral de Chile, Valdivia, Chile.
²⁵ Department of Anatomy, Physiology and Biochemistry, Swedish University of Agricultural Sciences, Post Office Box 7011, S-750 07, Uppsala, Sweden.
²⁶ Interdisciplinary Program in Bioinformatics, Seoul National University, Seoul 151-742, Republic of Korea. Cho and Kim Genomics, Seoul National University Research Park, Seoul 151-919, Republic of Korea. Department of Agricultural Biotechnology and Research Institute for Agriculture and Life Sciences, Seoul National University, Seoul 151-742, Republic of Korea.
²⁷ Interdisciplinary Program in Bioinformatics, Seoul National University, Seoul 151-742, Republic of Korea.
²⁸ Cho and Kim Genomics, Seoul National University Research Park, Seoul 151-919, Republic of Korea.
²⁹ State Key Laboratory for Agrobiotechnology, China Agricultural University, Beijing 100094, China.
³⁰ State Key Laboratory for Agrobiotechnology, China Agricultural University, Beijing 100094, China. College of Animal Science and Technology, China Agricultural University, Beijing 100094, China.
³¹ Organisms and Environment Division, Cardiff School of Biosciences, Cardiff University, Cardiff CF10 3AX, Wales, UK.
³² Organisms and Environment Division, Cardiff School of Biosciences, Cardiff University, Cardiff CF10 3AX, Wales, UK. Key Lab of Animal Ecology and Conservation Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101 China.
³³ International Wildlife Consultants, Carmarthen SA33 5YL, Wales, UK.
³⁴ Centre for Zoo and Wild Animal Health, Copenhagen Zoo, Roskildevej 38, DK-2000 Frederiksberg, Denmark.
³⁵ Department of Ecology and Evolutionary Biology, Tulane University, New Orleans, LA, USA. Museum of Natural Science, Louisiana State University, Baton Rouge, LA 70803, USA.
³⁶ The Genome Institute at Washington University, St. Louis, MO 63108, USA.
³⁷ College of Medicine and Forensics, Xi'an Jiaotong University, Xi'an, 710061, China.
³⁸ Institute for Genomics, Biocomputing and Biotechnology, Mississippi State University, Mississippi State, MS 39762, USA.
³⁹ Department of Biomolecular Engineering, University of California, Santa Cruz, CA 95064, USA.
⁴⁰ Theodosius Dobzhansky Center for Genome Bioinformatics, St. Petersburg State University, St. Petersburg, Russia. Nova Southeastern University Oceanographic Center 8000 N Ocean Drive, Dania, FL 33004, USA.
⁴¹ Smithsonian Conservation Biology Institute, National Zoological Park, 1500 Remount Road, Front Royal, VA 22630, USA.
⁴² Genetics Division, San Diego Zoo Institute for Conservation Research, 15600 San Pasqual Valley Road, Escondido, CA 92027, USA.
⁴³ Department of Vertebrate Zoology, MRC-116, National Museum of Natural History, Smithsonian Institution, Post Office Box 37012, Washington, DC 20013-7012, USA. Center for Macroecology, Evolution and Climate, the Natural History Museum of Denmark, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen O, Denmark.
⁴⁴ Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, 1 Beichen West Road, Chaoyang District, Beijing 100101, China. Swedish Species Information Centre, Swedish University of Agricultural Sciences, Box 7007, SE-750 07 Uppsala, Sweden.
⁴⁵ Center for Macroecology, Evolution and Climate, the Natural History Museum of Denmark, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen O, Denmark.
⁴⁶ Department of Biochemistry & Biophysics, University of California, San Francisco, CA 94158, USA.
⁴⁷ Department of Organismic and Evolutionary Biology and Museum of Comparative Zoology, Harvard University, 26 Oxford Street, Cambridge, MA 02138, USA.
⁴⁸ Department of Biology and Genetics Institute, University of Florida, Gainesville, FL 32611, USA.
⁴⁹ Center for Macroecology, Evolution and Climate, the Natural History Museum of Denmark, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen O, Denmark. Imperial College London, Grand Challenges in Ecosystems and the Environment Initiative, Silwood Park Campus, Ascot, Berkshire SL5 7PY, UK.
⁵⁰ 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.
⁵¹ Department of Biology, New Mexico State University, Box 30001 MSC 3AF, Las Cruces, NM 88003, USA.
⁵² China National GeneBank, Beijing Genomics Institute (BGI)-Shenzhen, Shenzhen, 518083, China. Macau University of Science and Technology, Avenida Wai long, Taipa, Macau 999078, China.
⁵³ Department of Neurobiology, Howard Hughes Medical Institute, Duke University Medical Center, Durham, NC 27710, USA. zhanggj@genomics.cn jarvis@neuro.duke.edu mtpgilbert@gmail.com wangj@genomics.cn.
⁵⁴ 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. zhanggj@genomics.cn jarvis@neuro.duke.edu mtpgilbert@gmail.com wangj@genomics.cn.
⁵⁵ China National GeneBank, Beijing Genomics Institute (BGI)-Shenzhen, Shenzhen, 518083, China. Macau University of Science and Technology, Avenida Wai long, Taipa, Macau 999078, 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. Department of Medicine, University of Hong Kong, Hong Kong. zhanggj@genomics.cn jarvis@neuro.duke.edu mtpgilbert@gmail.com wangj@genomics.cn.

PMID: 25504712
PMCID: PMC4390078
DOI: 10.1126/science.1251385

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.

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Figures

**Fig. 1. Avian family tree and genomes sequenced**
The phylogenomic relationships of the 48 avian genomes from (5), with Sanger-sequenced (black), high-coverage (dark red), and low-coverage (light red) genomes denoted.

**Fig. 2. Genome reduction and conservation in birds**
(A) Comparison of average size of introns, exons, and intergenic regions within avian, reptilian, and mammalian genomes. (B) Synteny plot and large segmental deletions between green anole chromosome 2 and multiple chicken chromosomes. Colored bars and lines indicate homologous blocks between two species; black bars indicate location of large avian-specific segmental deletions, which are enriched at the breakpoints of interchromosome rearrangements. (Bottom) An example of a large segmental deletion in birds (represented by ostrich genes). Homologous genes annotated in each species are shown in small boxes. The color spectrum represents the percent identity of homologous genes with the green anole. (C) Distribution of gene synteny percentages identified for phylogenetically independent species pairs of various divergence ages. Dots indicate the percentage of genes remaining in a syntenic block in pairwise comparisons between two avian or mammalian species. Box plots indicate that the overall distributions of the synteny percentages in birds and mammals are different (P value was calculated by using Wilcoxon rank sum test with phylogenetically independent species pairs). (D) Chromosomal organization of the α- and β-globin gene clusters in representative avian and mammalian taxa. These genes encode the α- and β-type subunits of tetrameric (α2β) hemoglobin isoforms that are expressed at different ontogenetic stages. In; the case of the α-like globin genes, birds and mammals share orthologous copies of the αD- and αA-globin genes. Likewise, the avian π-globin and the mammalian ζ-globin genes are 1:1 orthologs. In contrast, the genes in the avian and mammalian β-globin gene clusters are derived from independent duplications of one or more β-like globin genes that were inherited from the common ancestor of tetrapod vertebrates (90, 91).

**Fig. 3. Evolutionary rate and selection constraints**
(A) Substitution rate in each lineage was estimated by the comparison of fourfold degenerate (4d) sites in coding regions, in units of substitutions per site per million years. Waterbirds and landbirds are defined in (5). (B) Correlation between average substitution rates and number of species within different avian orders. Divergence times were estimates from (5).The fit line was derived from least square regression analysis, and the confidence interval was estimated by “stat_smooth” in R. The units of the x axis are numbers of substitutions per site per million years. The correlation figure with phylogenetically independent contrasts is provided in the supplementary materials. (C) Density map for comparison of conservation levels between pan-avian and pan-mammalian genomes, on the basis of the homologous genomic regions between birds and mammals. Conservation levels were quantified by means of PhastCons basewise conservation scores. (D) HCEs found in both mammalian and avian genomes (smaller pie piece) and those that are avian-specific (larger pie piece). (E) MID1 contains abundant avian-specific HCEs in the upstream and downstream regulatory regions. Many regulatory motif elements are identified in these avian-specific HCEs. Cons., conservation level.

**Fig. 4. Selection constraints on genes**
(A) Box plot for the distribution of dN/dS values of genes on avian macrochromosomes, microchromosomes, and the Z chromosome. P values were calculated with Wilcoxon rank sum tests. (B) GO categories in Neoaves, Galloanserae, and Palaeognathae showing clade-specific rapid evolutionary rates. Red bars, P value of significance; blue bars, number of genes in each GO.

**Fig. 5. Convergent molecular changes among vocal learning birds**
(A) Songbird brain diagram showing the specialized forebrain song-learning nuclei (yellow) that controls the production (HVC and RA) and acquisition (LMAN and Area X) of learned song (55). Gray arrows indicate connections between brain regions; red and blue (thick) arrows indicate relative numbers of genes with increased or decreased specialized expression in zebra finch song nuclei and with convergent accelerated coding sequences (left numbers of 66 total) or convergent amino acid substitutions (right numbers of 6). Genes expressed in more than one song nucleus are counted multiple times. RA, robust nucleus of the arcopallium; LMAN, lateral magnocellular nucleus of the anterior nidopallium; Area X, Area X of the striatum; and HVC, a letter-based name. (B) Classification of vocal learner-specific accelerated elements, compared with the background alignment of 15 avian species.

**Fig. 6. Genetic changes associated with ecological adaptations**
(A) Copy numbers of α- and β-keratins in humans, reptiles, and birds, including in aquatic birds, land birds, and domesticated birds. Definitions of aquatic and landbirds are provided in (5). (B) Pseudogenization events of the diet-related genes *AGT* and *GULO* along the avian phylogeny. (C) Density distribution of dN/dS values of the *OPN1sw1* gene for mammals (median, 0.21) and birds (median, 0.16). (D) dN/dS values of two plumage color–related genes (*GSTA2* and *SLC24A4*) show negative correlation with the color discriminability values (log transformation applied). The correlation figures with phylogenetically independent contrasts are provided in the supplementary materials.

See this image and copyright information in PMC

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1. Dyke G, Kaiser GW. Living Dinosaurs the Evolutionary History of Modern Birds. Hoboken, NJ: Wiley-Blackwell; 2011.
1. Feduccia A. Trends Ecol. Evol. 2003;18:172–176.
1. Jarvis ED, et al. Science. 2014;346:1320–1331. - PMC - PubMed

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[1] Gill F, Donsker D. IOC World Bird List (version 3.5) 2013

[2] Gill F, Donsker D. IOC World Bird List (version 3.5) 2013

[3] Chiappe LM, Witmer LM. Mesozoic Birds: Above the Heads of Dinosaurs. Berkeley, CA: Univ. California Press; 2002.

[4] Chiappe LM, Witmer LM. Mesozoic Birds: Above the Heads of Dinosaurs. Berkeley, CA: Univ. California Press; 2002.

[5] Dyke G, Kaiser GW. Living Dinosaurs the Evolutionary History of Modern Birds. Hoboken, NJ: Wiley-Blackwell; 2011.

[6] Dyke G, Kaiser GW. Living Dinosaurs the Evolutionary History of Modern Birds. Hoboken, NJ: Wiley-Blackwell; 2011.

[7] Feduccia A. Trends Ecol. Evol. 2003;18:172–176.

[8] Feduccia A. Trends Ecol. Evol. 2003;18:172–176.

[9] Jarvis ED, et al. Science. 2014;346:1320–1331. - PMC - PubMed

[10] Jarvis ED, et al. Science. 2014;346:1320–1331. - PMC - PubMed

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Comparative genomics reveals insights into avian genome evolution and adaptation

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Comparative genomics reveals insights into avian genome evolution and adaptation

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