Comparative genomics reveals insights into avian genome evolution and adaptation

Guojie Zhang; Cai Li; Qiye Li; Bo Li; Denis M. Larkin; Chul Lee; Jay F. Storz; Agostinho Antunes; Matthew J. Greenwold; Robert W. Meredith; Anders Ödeen; Jie Cui; Qi Zhou; Luohao Xu; Hailin Pan; Zongji Wang; Lijun Jin; Pei Zhang; Haofu Hu; Wei Yang; Jiang Hu; Jin Xiao; Zhikai Yang; Yang Liu; Qiaolin Xie; Hao Yu; Jinmin Lian; Ping Wen; Fang Zhang; Hui Li; Yongli Zeng; Zijun Xiong; Shiping Liu; Long Zhou; Zhiyong Huang; Na An; Jie Wang; Qiumei Zheng; Yingqi Xiong; Guangbiao Wang; Bo Wang; Jingjing Wang; Yu Fan; Rute Andreia Rodrigues da Fonseca; Luis Alonso Alfaro Nuñez; Mikkel Schubert; Ludovic Antoine Alexandre Orlando; Tobias Mourier; Jason T. Howard; Ganeshkumar Ganapathy; Andreas Pfenning; Osceola Whitney; Miriam V. Rivas; Erina Hara; Julia Smith; Marta Farré; Jitendra Narayan; Gancho Slavov; Michael N. Romanov; Rui Borges; João Paulo MacHado; Imran Khan; Mark S. Springer; John Gatesy; Federico G. Hoffmann; Juan C. Opazo; Olle Håstad; Roger H. Sawyer; Heebal Kim; Kyu Won Kim; Hyeon Jeong Kim; Seoae Cho; Ning Li; Yinhua Huang; Michael W. Bruford; Xiangjiang Zhan; Andrew Dixon; Mads F. Bertelsen; Elizabeth Derryberry; Wesley Warren; Richard K. Wilson; Shengbin Li; David A. Ray; Richard E. Green; Stephen J. O'Brien; Darren Griffin; Warren E. Johnson; David Haussler; Oliver A. Ryder; Eske Willerslev; Gary R. Graves; Per Alström; Jon Fjeldså; David P. Mindell; Scott V. Edwards; Edward L. Braun; Carsten Rahbek; David W. Burt; Peter Houde; Yong Zhang; Huanming Yang; Jian Wang; Erich D. Jarvis; M Thomas P Gilbert; Jun Wang

doi:10.1126/science.1251385

Comparative genomics reveals insights into avian genome evolution and adaptation

Guojie Zhang^*, Cai Li, Qiye Li, Bo Li, Denis M. Larkin, Chul Lee, Jay F. Storz, Agostinho Antunes, Matthew J. Greenwold, Robert W. Meredith, Anders Ödeen, Jie Cui, Qi Zhou, Luohao Xu, Hailin Pan, Zongji Wang, Lijun Jin, Pei Zhang, Haofu Hu, Wei YangJiang Hu, Jin Xiao, Zhikai Yang, Yang Liu, Qiaolin Xie, Hao Yu, Jinmin Lian, Ping Wen, Fang Zhang, Hui Li, Yongli Zeng, Zijun Xiong, Shiping Liu, Long Zhou, Zhiyong Huang, Na An, Jie Wang, Qiumei Zheng, Yingqi Xiong, Guangbiao Wang, Bo Wang, Jingjing Wang, Yu Fan, Rute Andreia Rodrigues da Fonseca, Luis Alonso Alfaro Nuñez, Mikkel Schubert, Ludovic Antoine Alexandre Orlando, Tobias Mourier, Jason T. Howard, Ganeshkumar Ganapathy, Andreas Pfenning, Osceola Whitney, Miriam V. Rivas, Erina Hara, Julia Smith, Marta Farré, Jitendra Narayan, Gancho Slavov, Michael N. Romanov, Rui Borges, João Paulo MacHado, Imran Khan, Mark S. Springer, John Gatesy, Federico G. Hoffmann, Juan C. Opazo, Olle Håstad, Roger H. Sawyer, Heebal Kim, Kyu Won Kim, Hyeon Jeong Kim, Seoae Cho, Ning Li, Yinhua Huang, Michael W. Bruford, Xiangjiang Zhan, Andrew Dixon, Mads F. Bertelsen, Elizabeth Derryberry, Wesley Warren, Richard K. Wilson, Shengbin Li, David A. Ray, Richard E. Green, Stephen J. O'Brien, Darren Griffin, Warren E. Johnson, David Haussler, Oliver A. Ryder, Eske Willerslev, Gary R. Graves, Per Alström, Jon Fjeldså, David P. Mindell, Scott V. Edwards, Edward L. Braun, Carsten Rahbek, David W. Burt, Peter Houde, Yong Zhang, Huanming Yang, Jian Wang, Erich D. Jarvis, M Thomas P Gilbert, Jun Wang

^*Corresponding author for this work

483 Citations (Scopus)

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.

Original language	English
Journal	Science
Volume	346
Issue number	6215
Pages (from-to)	1311-1320
Number of pages	10
ISSN	0036-8075
DOIs	https://doi.org/10.1126/science.1251385
Publication status	Published - 2014

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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., ... Wang, J. (2014). Comparative genomics reveals insights into avian genome evolution and adaptation. Science, 346(6215), 1311-1320. https://doi.org/10.1126/science.1251385

Zhang, G, Li, C, Li, Q, Li, B, Larkin, DM, Lee, C, Storz, JF, Antunes, A, Greenwold, MJ, Meredith, RW, 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, Rodrigues da Fonseca, RA, Alfaro Nuñez, LA, Schubert, M, Orlando, LAA, Mourier, T, Howard, JT, Ganapathy, G, Pfenning, A, Whitney, O, Rivas, MV, Hara, E, Smith, J, Farré, M, Narayan, J, Slavov, G, Romanov, MN, Borges, R, MacHado, JP, Khan, I, Springer, MS, Gatesy, J, Hoffmann, FG, Opazo, JC, Håstad, O, Sawyer, RH, Kim, H, Kim, KW, Kim, HJ, Cho, S, Li, N, Huang, Y, Bruford, MW, Zhan, X, Dixon, A, Bertelsen, MF, Derryberry, E, Warren, W, Wilson, RK, Li, S, Ray, DA, Green, RE, O'Brien, SJ, Griffin, D, Johnson, WE, Haussler, D, Ryder, OA, Willerslev, E, Graves, GR, Alström, P, Fjeldså, J, Mindell, DP, Edwards, SV, Braun, EL, Rahbek, C, Burt, DW, Houde, P, Zhang, Y, Yang, H, Wang, J, Jarvis, ED, Gilbert, MTP & Wang, J 2014, 'Comparative genomics reveals insights into avian genome evolution and adaptation', Science, vol. 346, no. 6215, pp. 1311-1320. https://doi.org/10.1126/science.1251385

@article{d2ddbede21bd4b5498dff85ce99e0629,

title = "Comparative genomics reveals insights into avian genome evolution and adaptation",

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.",

author = "Guojie Zhang and Cai Li and Qiye Li and Bo Li and Larkin, {Denis M.} and Chul Lee and Storz, {Jay F.} and Agostinho Antunes and Greenwold, {Matthew J.} and Meredith, {Robert W.} and Anders {\"O}deen and Jie Cui and Qi Zhou and Luohao Xu and Hailin Pan and Zongji Wang and Lijun Jin and Pei Zhang and Haofu Hu and Wei Yang and Jiang Hu and Jin Xiao and Zhikai Yang and Yang Liu and Qiaolin Xie and Hao Yu and Jinmin Lian and Ping Wen and Fang Zhang and Hui Li and Yongli Zeng and Zijun Xiong and Shiping Liu and Long Zhou and Zhiyong Huang and Na An and Jie Wang and Qiumei Zheng and Yingqi Xiong and Guangbiao Wang and Bo Wang and Jingjing Wang and Yu Fan and {Rodrigues da Fonseca}, {Rute Andreia} and {Alfaro Nu{\~n}ez}, {Luis Alonso} and Mikkel Schubert and Orlando, {Ludovic Antoine Alexandre} and Tobias Mourier and Howard, {Jason T.} and Ganeshkumar Ganapathy and Andreas Pfenning and Osceola Whitney and Rivas, {Miriam V.} and Erina Hara and Julia Smith and Marta Farr{\'e} and Jitendra Narayan and Gancho Slavov and Romanov, {Michael N.} and Rui Borges and MacHado, {Jo{\~a}o Paulo} and Imran Khan and Springer, {Mark S.} and John Gatesy and Hoffmann, {Federico G.} and Opazo, {Juan C.} and Olle H{\aa}stad and Sawyer, {Roger H.} and Heebal Kim and Kim, {Kyu Won} and Kim, {Hyeon Jeong} and Seoae Cho and Ning Li and Yinhua Huang and Bruford, {Michael W.} and Xiangjiang Zhan and Andrew Dixon and Bertelsen, {Mads F.} and Elizabeth Derryberry and Wesley Warren and Wilson, {Richard K.} and Shengbin Li and Ray, {David A.} and Green, {Richard E.} and O'Brien, {Stephen J.} and Darren Griffin and Johnson, {Warren E.} and David Haussler and Ryder, {Oliver A.} and Eske Willerslev and Graves, {Gary R.} and Per Alstr{\"o}m and Jon Fjelds{\aa} and Mindell, {David P.} and Edwards, {Scott V.} and Braun, {Edward L.} and Carsten Rahbek and Burt, {David W.} and Peter Houde and Yong Zhang and Huanming Yang and Jian Wang and Jarvis, {Erich D.} and Gilbert, {M Thomas P} and Jun Wang",

year = "2014",

doi = "10.1126/science.1251385",

language = "English",

volume = "346",

pages = "1311--1320",

journal = "Science",

issn = "0036-8075",

publisher = "American Association for the Advancement of Science",

number = "6215",

}

TY - JOUR

T1 - Comparative genomics reveals insights into avian genome evolution and adaptation

AU - Zhang, Guojie

AU - Li, Cai

AU - Li, Qiye

AU - Li, Bo

AU - Larkin, Denis M.

AU - Lee, Chul

AU - Storz, Jay F.

AU - Antunes, Agostinho

AU - Greenwold, Matthew J.

AU - Meredith, Robert W.

AU - Ödeen, Anders

AU - Cui, Jie

AU - Zhou, Qi

AU - Xu, Luohao

AU - Pan, Hailin

AU - Wang, Zongji

AU - Jin, Lijun

AU - Zhang, Pei

AU - Hu, Haofu

AU - Yang, Wei

AU - Hu, Jiang

AU - Xiao, Jin

AU - Yang, Zhikai

AU - Liu, Yang

AU - Xie, Qiaolin

AU - Yu, Hao

AU - Lian, Jinmin

AU - Wen, Ping

AU - Zhang, Fang

AU - Li, Hui

AU - Zeng, Yongli

AU - Xiong, Zijun

AU - Liu, Shiping

AU - Zhou, Long

AU - Huang, Zhiyong

AU - An, Na

AU - Wang, Jie

AU - Zheng, Qiumei

AU - Xiong, Yingqi

AU - Wang, Guangbiao

AU - Wang, Bo

AU - Wang, Jingjing

AU - Fan, Yu

AU - Rodrigues da Fonseca, Rute Andreia

AU - Alfaro Nuñez, Luis Alonso

AU - Schubert, Mikkel

AU - Orlando, Ludovic Antoine Alexandre

AU - Mourier, Tobias

AU - Howard, Jason T.

AU - Ganapathy, Ganeshkumar

AU - Pfenning, Andreas

AU - Whitney, Osceola

AU - Rivas, Miriam V.

AU - Hara, Erina

AU - Smith, Julia

AU - Farré, Marta

AU - Narayan, Jitendra

AU - Slavov, Gancho

AU - Romanov, Michael N.

AU - Borges, Rui

AU - MacHado, João Paulo

AU - Khan, Imran

AU - Springer, Mark S.

AU - Gatesy, John

AU - Hoffmann, Federico G.

AU - Opazo, Juan C.

AU - Håstad, Olle

AU - Sawyer, Roger H.

AU - Kim, Heebal

AU - Kim, Kyu Won

AU - Kim, Hyeon Jeong

AU - Cho, Seoae

AU - Li, Ning

AU - Huang, Yinhua

AU - Bruford, Michael W.

AU - Zhan, Xiangjiang

AU - Dixon, Andrew

AU - Bertelsen, Mads F.

AU - Derryberry, Elizabeth

AU - Warren, Wesley

AU - Wilson, Richard K.

AU - Li, Shengbin

AU - Ray, David A.

AU - Green, Richard E.

AU - O'Brien, Stephen J.

AU - Griffin, Darren

AU - Johnson, Warren E.

AU - Haussler, David

AU - Ryder, Oliver A.

AU - Willerslev, Eske

AU - Graves, Gary R.

AU - Alström, Per

AU - Fjeldså, Jon

AU - Mindell, David P.

AU - Edwards, Scott V.

AU - Braun, Edward L.

AU - Rahbek, Carsten

AU - Burt, David W.

AU - Houde, Peter

AU - Zhang, Yong

AU - Yang, Huanming

AU - Wang, Jian

AU - Jarvis, Erich D.

AU - Gilbert, M Thomas P

AU - Wang, Jun

PY - 2014

Y1 - 2014

N2 - 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.

AB - 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.

U2 - 10.1126/science.1251385

DO - 10.1126/science.1251385

M3 - Journal article

AN - SCOPUS:84917678595

SN - 0036-8075

VL - 346

SP - 1311

EP - 1320

JO - Science

JF - Science

IS - 6215

ER -

Comparative genomics reveals insights into avian genome evolution and adaptation

Abstract

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