Cited by 1,055Chromosomal and Genetic VariationsGenomics and Phylogenetic StudiesGenome Rearrangement Algorithms

Comparative genomics reveals insights into avian genome evolution and adaptation

Open access
Zhang, Guojie, Li, Cai, Li, Qiye, Li, Bo, Larkin, Denis M., Lee, Chul, Storz, Jay F., Antunes, Agostinho +132 more·2014·Science

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.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1126/science.1251385

Cites

22 of 22 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • The higher proportion of sequence for avians is consistent with a more conservative mode of genome evolution in avians that is influenced by lower repeat counts and denser gene content.

    “consistent with a more conservative mode of genome evolution in avians that is influenced by lower repeat counts and denser gene content33.”

    From Progressive Cactus is a multiple-genome aligner for the thousand-genome era (2020) · cites this paper as [33]

    The Results sections on selective constraints and conservative genome evolution report more slowly evolving regions and less genome shuffling in birds than in mammals. The broad-patterns Results also report fewer repeats and increased gene density, but the paper does not establish that those features influence the conservative mode of evolution. Page numbers are unavailable in our copy. (LLM, conf=0.84)

    Experimental — accuracy not yet measured
  • Multi-species genome alignments are a useful tool for analysis of species homology in large-scale comparative genomic projects.

    “Multi-species genome alignments are a useful tool for analysis of species homology in large-scale comparative genomic projects [12,13].”

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 78

  1. [2]Chiappe LM Witmer LM Mesozoic Birds: Above the Heads of Dinosaurs 2002 Berkeley, CA Univ. California Press
  2. [3]Dyke G Kaiser GW Living Dinosaurs the Evolutionary History of Modern Birds 2011 Hoboken, NJ Wiley-Blackwell
  3. [5]Jarvis ED Science 2014 346 1320 1331 25504713 PMC4405904
  4. [6]Holt BG Science 2013 339 74 78 23258408
  5. [7]Jetz W Thomas GH Joy JB Hartmann K Mooers AO Nature 2012 491 444 448 23123857
  6. [8]Zeigler H Marler PE Behavioral Neurobiology of Birdsong 2002 12 New York, NY, US Hunter College, City University of New York this volume is the result of the aforementioned conference which was one of an annual symposium series sponsored by the Hunter College Gene Center. (2004).
  7. [9]Stattersfield AJ Crosby MJ Long AJ Wege DC Endemic Bird Areas of the World: Priorities for Conservation. BirdLife Conservation 1998 Cambridge, UK BirdLife International
  8. [10]Alexander DJ Vet. Microbiol 2000 74 3 13 10799774
  9. [13]Warren WC Nature 2010 464 757 762 20360741 PMC3187626
  10. [14]Huang Y Nat. Genet 2013 45 776 783 23749191 PMC4003391
  11. [15]Zhan X Nat. Genet 2013 45 563 566 23525076
  12. [16]Shapiro MD Science 2013 339 1063 1067 23371554 PMC3778192
  13. [17]Dickinson E Remsen J The Howard and Moore Complete Checklist of the Birds of the World 2013 Eastbourne, UK Aves Press
  14. [19]Zhang G GigaScience 2014 3 26 25671091 PMC4322804
  15. [22]Zhou Q Science 2014 346 1246338 25504727 PMC6445272
  16. [23]Lander ES Nature 2001 409 860 921 11237011
  17. [24]Green RE Science 2014 346 1254449 25504731 PMC4386873
  18. [25]Hughes AL Hughes MK Nature 1995 377 391 7566113
  19. [26]Rho M Genome Biol. Evol 2009 1 2 12 20333172 PMC2817402
  20. [27]Morand S Ricklefs RE Trends Genet 2001 17 567 568 11642250
  21. [28]Waltari E Edwards SV Am. Nat 2002 160 539 552 18707506
  22. [29]Kidwell MG Genetica 2002 115 49 63 12188048
  23. [30]Feschotte C Pritham EJ Annu. Rev. Genet 2007 41 331 368 18076328 PMC2167627
  24. [31]Lynch M Conery JS J. Struct. Funct. Genomics 2003 3 35 44 12836683
  25. [32]Sela N Kim E Ast G Genome Biol 2010 11 R59 20525173 PMC2911107
  26. [33]Böhne A Brunet F Galiana-Arnoux D Schultheis C Volff JN Chromosome Res 2008 16 203 215 18293113
  27. [34]Zhang Q Edwards SV Genome Biol. Evol 2012 4 1033 1043 22930760 PMC3490418
  28. [35]Organ CL Shedlock AM Meade A Pagel M Edwards SV Nature 2007 446 180 184 17344851
  29. [36]Hughes AL Friedman R Mol. Biol. Evol 2008 25 2681 2688 18820253 PMC2721554
  30. [37]Griffin DK Robertson LBW Tempest HG Skinner BM Cytogenet. Genome Res 2007 117 64 77 17675846
  31. [38]Bradnam KR GigaScience 2013 2 10 23870653 PMC3844414
  32. [39]Kim J Proc. Natl. Acad. Sci. U.S.A 2013 110 1785 1790 23307812 PMC3562798
  33. [40]Hoffmann FG Opazo JC Storz JF Mol. Biol. Evol 2012 29 303 312 21965344 PMC3245541
  34. [41]Hoffmann FG Opazo JC Storz JF Mol. Biol. Evol 2008 25 591 602 18178968
  35. [42]Grispo MT J. Biol. Chem 2012 287 37647 37658 22962007 PMC3488042
  36. [43]Baer CF Miyamoto MM Denver DR Nat. Rev. Genet 2007 8 619 631 17637734
  37. [44]Venditti C Pagel M Trends Ecol. Evol 2010 25 14 20 19720426
  38. [45]Siepel A Genome Res 2005 15 1034 1050 16024819 PMC1182216
  39. [46]Lindblad-Toh K Nature 2011 478 476 482 21993624 PMC3207357
  40. [47]Nabholz B Glémin S Galtier N BMC Evol. Biol 2009 9 54 19284537 PMC2660308
  41. [48]Lathrop WF Carmichael EP Myles DG Primakoff P J. Cell Biol 1990 111 2939 2949 2269661 PMC2116349
  42. [49]Swanson WJ Vacquier VD Nat. Rev. Genet 2002 3 137 144 11836507
  43. [50]Pennacchio LA Nature 2006 444 499 502 17086198
  44. [51]ENCODE Project Consortium Nature 2012 489 57 74 22955616 PMC3439153
  45. [52]Mank JE Axelsson E Ellegren H Genome Res 2007 17 618 624 17416747 PMC1855182
  46. [53]Axelsson E Webster MT Smith NGC Burt DW Ellegren H Genome Res 2005 15 120 125 15590944 PMC540272
  47. [54]Suh A Nat. Commun 2011 2 443 21863010 PMC3265382
  48. [55]Jarvis ED Ann. N. Y. Acad. Sci 2004 1016 749 777 15313804 PMC2485240
  49. [56]Whitney O Science 2014 346 1256780 25504732 PMC4359888
  50. [57]Pfenning AR Science 2014 346 1256846 25504733 PMC4385736
  51. [58]Karten HJ J. Comp. Neurol 2013 521 3702 3715 23896990 PMC3931548
  52. [59]Hubisz MJ Pollard KS Siepel A Brief. Bioinform 2011 12 41 51 21278375 PMC3030812
  53. [60]Dumont ER Proc. Biol. Sci 2010 277 2193 2198 20236981 PMC2880151
  54. [61]Gutzwiller SC Su A O’Connor PM Anat. Rec 2013 296 867 876 23554179
  55. [62]Duncker HR Respir. Physiol. Neurobiol 2004 144 111 124 15556096
  56. [63]West JB Watson RR Fu Z Respir. Physiol. Neurobiol 2007 157 382 390 17222589 PMC2681264
  57. [65]Haake AR König G Sawyer RH Dev. Biol 1984 106 406 413 6209181
  58. [66]Ross-Ibarra J Am. Nat 2004 163 105 112 14767840
  59. [67]Blirt A Bell G Nature 1987 326 803 805 3574451
  60. [68]Louchart A Viriot L Trends Ecol. Evol 2011 26 663 673 21978465
  61. [69]Livezey BC Zusi RL Zool. J. Linn. Soc 2007 149 1 95 18784798 PMC2517308
  62. [71]Meredith RW Zhang G Gilbert MTP Jarvis ED Springer MS Science 2014 346 1254390 25504730
  63. [72]Birdsey GM Lewin J Cunningham AA Bruford MW Danpure CJ Mol. Biol. Evol 2004 21 632 646 14739251
  64. [73]Chatterjee IB Science 1973 182 1271 1272 4752221
  65. [74]Cui J Yuan X Wang L Jones G Zhang S PLOS ONE 2011 6 e27114 22069493 PMC3206078
  66. [75]Cui J Pan Y-H Zhang Y Jones G Zhang S Mol. Biol. Evol 2011 28 1025 1031 21037206
  67. [76]Davies WIL Collin SP Hunt DM Mol. Ecol 2012 21 3121 3158 22650357
  68. [77]Pires SS Proc. Biol. Sci 2007 274 2791 2799 17785267 PMC3227130
  69. [79]Ödeen A Håstad O Alström P BMC Evol. Biol 2011 11 313 22024316 PMC3225180
  70. [81]Guraya SS Ovarian Follicles in Reptiles and Birds 1989 Berlin, Germany Springer-Verlag
  71. [82]Zheng X Nature 2013 495 507 511 23503663
  72. [83]Jo M Curry TE Jr Biol. Reprod 2004 71 1796 1806 15286033
  73. [84]Goodarzi MO Antoine HJ Azziz R J. Clin. Endocrinol. Metab 2007 92 2659 2664 17426092
  74. [85]Birkhead TR Møller AP Sperm competition and sexual selection 1998 Academic Press
  75. [88]Mateos C Carranza J Anim. Behav 1997 54 1205 1214 9398373
  76. [89]Quinlan AR Hall IM Trends Genet 2012 28 43 53 22094265 PMC3249479
  77. [90]Storz JF Opazo JC Hoffmann FG Mol. Phylogenet. Evol 2013 66 469 478 22846683 PMC4306229
  78. [91]Hoffmann FG Storz JF Gorr TA Opazo JC Mol. Biol. Evol 2010 27 1126 1138 20047955 PMC2877528

Cited by

Sorted by citations

Authors
Zhang, G., Li, C., Li, Q., Li, B., Larkin, D. M., Lee, C., Storz, J. F., Antunes, A., Greenwold, M. J., Meredith, R. W., Ödeen, A., Cui, J., Zhou, Q., Xu, L., Pan, H., Wang, Z., Jin, L., Zhang, P., Hu, H., Yang, W., Hu, J., Xiao, J., Yang, Z., Liu, Y., Xie, Q., Yu, H., Lian, J., Wen, P., Zhang, F., Li, H., Zeng, Y., Xiong, Z., Liu, S., Zhou, L., Huang, Z., An, N., Wang, J., Zheng, Q., Xiong, Y., Wang, G., Wang, B., Wang, J., Fan, Y., da Fonseca, R. R., Alfaro-Núñez, A., Schubert, M., Orlando, L., Mourier, T., Howard, J. T., Ganapathy, G., Pfenning, A., Whitney, O., Rivas, M. V., Hara, E., Smith, J., Farré, M., Narayan, J., Slavov, G., Romanov, M. N., Borges, R., Machado, J. P., Khan, I., Springer, M. S., Gatesy, J., Hoffmann, F. G., Opazo, J. C., Håstad, O., Sawyer, R. H., Kim, H., Kim, K.-W., Kim, H. J., Cho, S., Li, N., Huang, Y., Bruford, M. W., Zhan, X., Dixon, A., Bertelsen, M. F., Derryberry, E., Warren, W., Wilson, R. K., Li, S., Ray, D. A., Green, R. E., O’Brien, S. J., Griffin, D., Johnson, W. E., Haussler, D., Ryder, O. A., Willerslev, E., Graves, G. R., Alström, P., Fjeldså, J., Mindell, D. P., Edwards, S. V., Braun, E. L., Rahbek, C., Burt, D. W., Houde, P., Zhang, Y., Yang, H., Wang, J., Avian Genome Consortium, Jarvis, E. D., Gilbert, M. T. P., Wang, J., Ye, C., Liang, S., Yan, Z., Zepeda, M. L., Campos, P. F., Velazquez, A. M. V., Samaniego, J. A., Avila-Arcos, M., Martin, M. D., Barnett, R., Ribeiro, A. M., Mello, C. V., Lovell, P. V., Almeida, D., Maldonado, E., Pereira, J., Sunagar, K., Philip, S., Dominguez-Bello, M. G., Bunce, M., Lambert, D., Brumfield, R. T., Sheldon, F. H., Holmes, E. C., Gardner, P. P., Steeves, T. E., Stadler, P. F., Burge, S. W., Lyons, E., Smith, J., McCarthy, F., Pitel, F., Rhoads, D., & Froman, D. P.
Affiliations
  • BGI Group (China) (CN)
  • University of London (GB)
  • Seoul National University (KR)
  • University of Nebraska–Lincoln (US)
  • Universidade do Porto (PT)
  • University of South Carolina (US)
  • Montclair State University (US)
  • Uppsala University (SE)
  • The University of Sydney (AU)
  • University of California, Berkeley (US)
  • China National GeneBank, Beijing Genomics Institute (BGI)–Shenzhen, Shenzhen, 518083, China.
  • Kunming Institute of Zoology (CN)
  • Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Øster Voldgade 5-7, 1350 Copenhagen, Denmark.
  • University of Copenhagen (DK)
  • Howard Hughes Medical Institute (US)
  • Aberystwyth University (GB)
  • University of Kent (GB)
  • University of California, Riverside (US)
  • Mississippi State University (US)
  • Austral University of Chile (CL)
  • Swedish University of Agricultural Sciences (SE)
  • 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.
  • China Agricultural University (CN)
  • Cardiff University (GB)
  • Chinese Academy of Sciences (CN)
  • International Wildlife Consultants (United Kingdom) (GB)
  • Copenhagen Zoo (DK)
  • Tulane University (US)
  • Washington University in St. Louis (US)
  • Xi'an Jiaotong University (CN)
  • University of California, Santa Cruz (US)
  • St Petersburg University (RU)
  • Smithsonian Conservation Biology Institute (US)
  • San Diego Zoo Institute for Conservation Research (US)
  • Smithsonian Institution (US)
  • University of California, San Francisco (US)
  • Harvard University (US)
  • University of Florida (US)
  • Roslin Institute (GB)
  • New Mexico State University (US)
Corresponding author
  • Zhang, Guojie
  • Li, Cai
  • Jarvis, Erich D.
  • Gilbert, M. Thomas P.
  • Wang, Jun
Venue
Science
Published
2014-12-12
Volume
346
Issue
6215
Pages
1311-1320
ISSN
  • 0036-8075 (ISSN-L)
  • 1095-9203
OpenAlex
W2167406239
Cited by
1,055
References
22
Citations by year
2026: 63 · 2025: 58 · 2024: 72 · 2023: 78 · 2022: 83 · 2021: 129 · 2020: 95 · 2019: 114 · 2018: 89 · 2017: 90 · 2016: 83 · 2015: 80 · 2014: 20
FWCI
97.39
Type
journal article
Language
en
Open access
Locations
  • Science (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
  • Kent Academic Repository (University of Kent) (acceptedVersion)
  • Civil War Book Review (submittedVersion)
  • RVC Research Online (Royal Veterinary College) (submittedVersion, cc-by)
  • Lincoln (University of Nebraska) (submittedVersion)
  • NSUWorks (Nova Southeastern University) (submittedVersion)
  • HAL (submittedVersion)
  • DukeSpace (Duke University) (submittedVersion)
  • DukeSpace (Duke University) (submittedVersion, cc-by-nc-nd)
  • eScholarship (California Digital Library) (submittedVersion)
  • eSpace (Curtin University) (submittedVersion)
  • ORCA Online Research @Cardiff (Cardiff University) (submittedVersion)
  • Research at the University of Copenhagen (University of Copenhagen) (submittedVersion)
  • DSpace Repository (Smithsonian) (submittedVersion)
  • Griffith Research Online (submittedVersion)
Funders
  • Howard Hughes Medical Institute
  • Villum Fonden (00007370)
  • National Research Foundation
  • Danmarks Grundforskningsfond (DNRF94)
  • Lundbeckfonden (R109-2012-9995, R70-2010-6286, R155-2013-16338, R52‐A5062, R38-2008-3048, R24-2008-2527)
  • Danmarks Frie Forskningsfond (10‐081390)
  • H. Lundbeck A/S
  • National Institutes of Health (DP1OD000448)
  • Biotechnology and Biological Sciences Research Council (BB/J010170/2, BB/K008226/2, BB/J010170/1, BB/K008226/1)
  • National Heart, Lung, and Blood Institute (R01HL087216)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Chromosomal and Genetic Variations
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genome Rearrangement Algorithms
Keywords
avian genome evolution, comparative genomics, genome size reduction, segmental deletion, gene loss, evolutionary stasis, synteny, chromosome structure, non-neutral evolution, non-coding regions, convergent evolution, lifestyle adaptation, genomic diversity
MeSH terms
Adaptation, Physiological, Animals, Birds, Diet, Biological Evolution, Female, Flight, Animal, Genes, Male, Phylogeny, Reproduction, Selection, Genetic, Genetic Variation, Vision, Ocular, Vocalization, Animal, Genome, Conserved Sequence, Sequence Analysis, DNA, Evolution, Molecular, Genomics, Synteny, Biodiversity, Molecular Sequence Annotation

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review