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

Erich D. Jarvis; Siavash Mirarab; Andre J. Aberer; Bo Li; Peter Houde; Cai Li; Simon Y W Ho; Brant C. Faircloth; Benoit Nabholz; Jason T. Howard; Alexander Suh; Claudia C. Weber; Rute Andreia Rodrigues da Fonseca; Jianwen Li; Fang Zhang; Hui Li; Long Zhou; Nitish Narula; Liang Liu; Ganesh Ganapathy; Bastien Boussau; Md Shamsuzzoha Bayzid; Volodymyr Zavidovych; Sankar Subramanian; Toni Gabaldón; Salvador Capella-Gutiérrez; Jaime Huerta-Cepas; Bhanu Rekepalli; Kasper Munch Terkelsen; Mikkel Heide Schierup; Bent Erik Kramer Lindow; Wesley C. Warren; David Ray; Richard E. Green; Michael W. Bruford; Xiangjiang Zhan; Andrew Dixon; Shengbin Li; Ning Li; Yinhua Huang; Elizabeth P. Derryberry; Mads Frost Bertelsen; Frederick H. Sheldon; Robb T. Brumfield; Claudio V. Mello; Peter V. Lovell; Morgan Wirthlin; Maria Paula Cruz Schneider; Francisco Prosdocimi; Jose Alfredo Samaniego Castruita; Amhed Missael Vargas Velazquez; Luis Alonso Alfaro Nuñez; Paula Campos; Bent Petersen; Thomas Sicheritz-Ponten; An Pas; Tom Bailey; Paul Scofield; Michael Bunce; David M. Lambert; Qi Zhou; Polina Perelman; Amy C. Driskell; Beth Shapiro; Zijun Xiong; Yongli Zeng; Shiping Liu; Zhenyu Li; Binghang Liu; Kui Wu; Jin Xiao; Xiong Yinqi; Qiuemei Zheng; Yong Zhang; Huanming Yang; Jian Wang; Linnea Smeds; Frank E. Rheindt; Michael Braun; Jon Fjeldså; Ludovic Antoine Alexandre Orlando; F. Keith Barker; Knud Andreas Jønsson; Warren Johnson; Klaus Peter Koepfli; Stephen O'Brien; David Haussler; Oliver A. Ryder; Carsten Rahbek; Eske Willerslev; Gary R. Graves; Travis C. Glenn; John McCormack; Dave Burt; Hans Ellegren; Per Alström; Scott V. Edwards; Alexandros Stamatakis; David P. Mindell; Joel Cracraft; Edward L. Braun; Tandy Warnow; Jun Wang; M Thomas P Gilbert; Guojie Zhang

doi:10.1126/science.1253451

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

Erich D. Jarvis^*, Siavash Mirarab, Andre J. Aberer, Bo Li, Peter Houde, Cai Li, Simon Y W Ho, Brant C. Faircloth, Benoit Nabholz, Jason T. Howard, Alexander Suh, Claudia C. Weber, Rute Andreia Rodrigues da Fonseca, Jianwen Li, Fang Zhang, Hui Li, Long Zhou, Nitish Narula, Liang Liu, Ganesh GanapathyBastien Boussau, Md Shamsuzzoha Bayzid, Volodymyr Zavidovych, Sankar Subramanian, Toni Gabaldón, Salvador Capella-Gutiérrez, Jaime Huerta-Cepas, Bhanu Rekepalli, Kasper Munch Terkelsen, Mikkel Heide Schierup, Bent Erik Kramer Lindow, Wesley C. Warren, David Ray, Richard E. Green, Michael W. Bruford, Xiangjiang Zhan, Andrew Dixon, Shengbin Li, Ning Li, Yinhua Huang, Elizabeth P. Derryberry, Mads Frost Bertelsen, Frederick H. Sheldon, Robb T. Brumfield, Claudio V. Mello, Peter V. Lovell, Morgan Wirthlin, Maria Paula Cruz Schneider, Francisco Prosdocimi, Jose Alfredo Samaniego Castruita, Amhed Missael Vargas Velazquez, Luis Alonso Alfaro Nuñez, Paula Campos, Bent Petersen, Thomas Sicheritz-Ponten, An Pas, Tom Bailey, Paul Scofield, Michael Bunce, David M. Lambert, Qi Zhou, Polina Perelman, Amy C. Driskell, Beth Shapiro, Zijun Xiong, Yongli Zeng, Shiping Liu, Zhenyu Li, Binghang Liu, Kui Wu, Jin Xiao, Xiong Yinqi, Qiuemei Zheng, Yong Zhang, Huanming Yang, Jian Wang, Linnea Smeds, Frank E. Rheindt, Michael Braun, Jon Fjeldså, Ludovic Antoine Alexandre Orlando, F. Keith Barker, Knud Andreas Jønsson, Warren Johnson, Klaus Peter Koepfli, Stephen O'Brien, David Haussler, Oliver A. Ryder, Carsten Rahbek, Eske Willerslev, Gary R. Graves, Travis C. Glenn, John McCormack, Dave Burt, Hans Ellegren, Per Alström, Scott V. Edwards, Alexandros Stamatakis, David P. Mindell, Joel Cracraft, Edward L. Braun, Tandy Warnow, Jun Wang, M Thomas P Gilbert, Guojie Zhang

^*Corresponding author for this work

958 Citations (Scopus)

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.

Original language	English
Journal	Science
Volume	346
Issue number	6215
Pages (from-to)	1320-1331
Number of pages	12
ISSN	0036-8075
DOIs	https://doi.org/10.1126/science.1253451
Publication status	Published - 2014

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Jarvis, E. D., Mirarab, S., Aberer, A. J., Li, B., Houde, P., Li, C., Ho, S. Y. W., Faircloth, B. C., Nabholz, B., Howard, J. T., Suh, A., Weber, C. C., Rodrigues da Fonseca, R. A., Li, J., Zhang, F., Li, H., Zhou, L., Narula, N., Liu, L., ... Zhang, G. (2014). Whole-genome analyses resolve early branches in the tree of life of modern birds. Science, 346(6215), 1320-1331. https://doi.org/10.1126/science.1253451

Jarvis, ED, Mirarab, S, Aberer, AJ, Li, B, Houde, P, Li, C, Ho, SYW, Faircloth, BC, Nabholz, B, Howard, JT, Suh, A, Weber, CC, Rodrigues da Fonseca, RA, Li, J, Zhang, F, Li, H, Zhou, L, Narula, N, Liu, L, Ganapathy, G, Boussau, B, Bayzid, MS, Zavidovych, V, Subramanian, S, Gabaldón, T, Capella-Gutiérrez, S, Huerta-Cepas, J, Rekepalli, B, Terkelsen, KM, Schierup, MH, Lindow, BEK, Warren, WC, Ray, D, Green, RE, Bruford, MW, Zhan, X, Dixon, A, Li, S, Li, N, Huang, Y, Derryberry, EP, Bertelsen, MF, Sheldon, FH, Brumfield, RT, Mello, CV, Lovell, PV, Wirthlin, M, Schneider, MPC, Prosdocimi, F, Samaniego Castruita, JA, Velazquez, AMV, Alfaro Nuñez, LA, Campos, P, Petersen, B, Sicheritz-Ponten, T, Pas, A, Bailey, T, Scofield, P, Bunce, M, Lambert, DM, Zhou, Q, Perelman, P, Driskell, AC, Shapiro, B, Xiong, Z, Zeng, Y, Liu, S, Li, Z, Liu, B, Wu, K, Xiao, J, Yinqi, X, Zheng, Q, Zhang, Y, Yang, H, Wang, J, Smeds, L, Rheindt, FE, Braun, M, Fjeldså, J, Orlando, LAA, Barker, FK, Jønsson, KA, Johnson, W, Koepfli, KP, O'Brien, S, Haussler, D, Ryder, OA, Rahbek, C , Willerslev, E, Graves, GR, Glenn, TC, McCormack, J, Burt, D, Ellegren, H, Alström, P, Edwards, SV, Stamatakis, A, Mindell, DP, Cracraft, J, Braun, EL, Warnow, T, Wang, J, Gilbert, MTP & Zhang, G 2014, 'Whole-genome analyses resolve early branches in the tree of life of modern birds', Science, vol. 346, no. 6215, pp. 1320-1331. https://doi.org/10.1126/science.1253451

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title = "Whole-genome analyses resolve early branches in the tree of life of modern birds",

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.",

author = "Jarvis, {Erich D.} and Siavash Mirarab and Aberer, {Andre J.} and Bo Li and Peter Houde and Cai Li and Ho, {Simon Y W} and Faircloth, {Brant C.} and Benoit Nabholz and Howard, {Jason T.} and Alexander Suh and Weber, {Claudia C.} and {Rodrigues da Fonseca}, {Rute Andreia} and Jianwen Li and Fang Zhang and Hui Li and Long Zhou and Nitish Narula and Liang Liu and Ganesh Ganapathy and Bastien Boussau and Bayzid, {Md Shamsuzzoha} and Volodymyr Zavidovych and Sankar Subramanian and Toni Gabald{\'o}n and Salvador Capella-Guti{\'e}rrez and Jaime Huerta-Cepas and Bhanu Rekepalli and Terkelsen, {Kasper Munch} and Schierup, {Mikkel Heide} and Lindow, {Bent Erik Kramer} and Warren, {Wesley C.} and David Ray and Green, {Richard E.} and Bruford, {Michael W.} and Xiangjiang Zhan and Andrew Dixon and Shengbin Li and Ning Li and Yinhua Huang and Derryberry, {Elizabeth P.} and Bertelsen, {Mads Frost} and Sheldon, {Frederick H.} and Brumfield, {Robb T.} and Mello, {Claudio V.} and Lovell, {Peter V.} and Morgan Wirthlin and Schneider, {Maria Paula Cruz} and Francisco Prosdocimi and {Samaniego Castruita}, {Jose Alfredo} and Velazquez, {Amhed Missael Vargas} and {Alfaro Nu{\~n}ez}, {Luis Alonso} and Paula Campos and Bent Petersen and Thomas Sicheritz-Ponten and An Pas and Tom Bailey and Paul Scofield and Michael Bunce and Lambert, {David M.} and Qi Zhou and Polina Perelman and Driskell, {Amy C.} and Beth Shapiro and Zijun Xiong and Yongli Zeng and Shiping Liu and Zhenyu Li and Binghang Liu and Kui Wu and Jin Xiao and Xiong Yinqi and Qiuemei Zheng and Yong Zhang and Huanming Yang and Jian Wang and Linnea Smeds and Rheindt, {Frank E.} and Michael Braun and Jon Fjelds{\aa} and Orlando, {Ludovic Antoine Alexandre} and Barker, {F. Keith} and J{\o}nsson, {Knud Andreas} and Warren Johnson and Koepfli, {Klaus Peter} and Stephen O'Brien and David Haussler and Ryder, {Oliver A.} and Carsten Rahbek and Eske Willerslev and Graves, {Gary R.} and Glenn, {Travis C.} and John McCormack and Dave Burt and Hans Ellegren and Per Alstr{\"o}m and Edwards, {Scott V.} and Alexandros Stamatakis and Mindell, {David P.} and Joel Cracraft and Braun, {Edward L.} and Tandy Warnow and Jun Wang and Gilbert, {M Thomas P} and Guojie Zhang",

year = "2014",

doi = "10.1126/science.1253451",

language = "English",

volume = "346",

pages = "1320--1331",

journal = "Science",

issn = "0036-8075",

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

number = "6215",

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TY - JOUR

T1 - Whole-genome analyses resolve early branches in the tree of life of modern birds

AU - Jarvis, Erich D.

AU - Mirarab, Siavash

AU - Aberer, Andre J.

AU - Li, Bo

AU - Houde, Peter

AU - Li, Cai

AU - Ho, Simon Y W

AU - Faircloth, Brant C.

AU - Nabholz, Benoit

AU - Howard, Jason T.

AU - Suh, Alexander

AU - Weber, Claudia C.

AU - Rodrigues da Fonseca, Rute Andreia

AU - Li, Jianwen

AU - Zhang, Fang

AU - Li, Hui

AU - Zhou, Long

AU - Narula, Nitish

AU - Liu, Liang

AU - Ganapathy, Ganesh

AU - Boussau, Bastien

AU - Bayzid, Md Shamsuzzoha

AU - Zavidovych, Volodymyr

AU - Subramanian, Sankar

AU - Gabaldón, Toni

AU - Capella-Gutiérrez, Salvador

AU - Huerta-Cepas, Jaime

AU - Rekepalli, Bhanu

AU - Terkelsen, Kasper Munch

AU - Schierup, Mikkel Heide

AU - Lindow, Bent Erik Kramer

AU - Warren, Wesley C.

AU - Ray, David

AU - Green, Richard E.

AU - Bruford, Michael W.

AU - Zhan, Xiangjiang

AU - Dixon, Andrew

AU - Li, Shengbin

AU - Li, Ning

AU - Huang, Yinhua

AU - Derryberry, Elizabeth P.

AU - Bertelsen, Mads Frost

AU - Sheldon, Frederick H.

AU - Brumfield, Robb T.

AU - Mello, Claudio V.

AU - Lovell, Peter V.

AU - Wirthlin, Morgan

AU - Schneider, Maria Paula Cruz

AU - Prosdocimi, Francisco

AU - Samaniego Castruita, Jose Alfredo

AU - Velazquez, Amhed Missael Vargas

AU - Alfaro Nuñez, Luis Alonso

AU - Campos, Paula

AU - Petersen, Bent

AU - Sicheritz-Ponten, Thomas

AU - Pas, An

AU - Bailey, Tom

AU - Scofield, Paul

AU - Bunce, Michael

AU - Lambert, David M.

AU - Zhou, Qi

AU - Perelman, Polina

AU - Driskell, Amy C.

AU - Shapiro, Beth

AU - Xiong, Zijun

AU - Zeng, Yongli

AU - Liu, Shiping

AU - Li, Zhenyu

AU - Liu, Binghang

AU - Wu, Kui

AU - Xiao, Jin

AU - Yinqi, Xiong

AU - Zheng, Qiuemei

AU - Zhang, Yong

AU - Yang, Huanming

AU - Wang, Jian

AU - Smeds, Linnea

AU - Rheindt, Frank E.

AU - Braun, Michael

AU - Fjeldså, Jon

AU - Orlando, Ludovic Antoine Alexandre

AU - Barker, F. Keith

AU - Jønsson, Knud Andreas

AU - Johnson, Warren

AU - Koepfli, Klaus Peter

AU - O'Brien, Stephen

AU - Haussler, David

AU - Ryder, Oliver A.

AU - Rahbek, Carsten

AU - Willerslev, Eske

AU - Graves, Gary R.

AU - Glenn, Travis C.

AU - McCormack, John

AU - Burt, Dave

AU - Ellegren, Hans

AU - Alström, Per

AU - Edwards, Scott V.

AU - Stamatakis, Alexandros

AU - Mindell, David P.

AU - Cracraft, Joel

AU - Braun, Edward L.

AU - Warnow, Tandy

AU - Wang, Jun

AU - Gilbert, M Thomas P

AU - Zhang, Guojie

PY - 2014

Y1 - 2014

N2 - 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.

AB - 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.

U2 - 10.1126/science.1253451

DO - 10.1126/science.1253451

M3 - Journal article

AN - SCOPUS:84917708482

SN - 0036-8075

VL - 346

SP - 1320

EP - 1331

JO - Science

JF - Science

IS - 6215

ER -

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

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