The African coelacanth genome provides insights into tetrapod evolution

Chris T. Amemiya; Jessica Alfoldi; Alison P. Lee; Shaohua Fan; Hervé Philippe; Iain MacCallum; Ingo Braasch; Tereza Manousaki; Igor Schneider; Nicolas Rohner; Chris Organ; Domitille Chalopin; Jeramiah J. Smith; Mark Robinson; Rosemary A. Dorrington; Marco Gerdol; Bronwen Aken; Maria Assunta Biscotti; Marco Barucca; Denis Baurain; Aaron M. Berlin; Gregory L. Blatch; Francesco Buonocore; Thorsten Burmester; Michael S. Campbell; Adriana Canapa; John P. Cannon; Alan Christoffels; Gianluca De Moro; Adrienne L. Edkins; Lin Fan; Anna Maria Fausto; Nathalie Feiner; Mariko Forconi; Junaid Gamieldien; Sante Gnerre; Andreas Gnirke; Jared V. Goldstone; Wilfried Haerty; Mark E. Hahn; Uljana Hesse; Steve Hoffmann; Jeremy Johnson; Sibel I. Karchner; Shigehiro Kuraku; Marcia Lara; Joshua Z. Levin; Gary W. Litman; Evan Mauceli; Tsutomu Miyake; M. Gail Mueller; David R. Nelson; Anne Nitsche; Ettore Olmo; Tatsuya Ota; Alberto Pallavicini; Sumir Panji; Barbara Picone; Chris P. Ponting; Sonja J. Prohaska; Dariusz Przybylski; Nil Ratan Saha; Vydianathan Ravi; Filipe J. Ribeiro; Tatjana Sauka-Spengler; Giuseppe Scapigliati; Stephen M.J. Searle; Ted Sharpe; Oleg Simakov; Peter F. Stadler; John J. Stegeman; Kenta Sumiyama; Diana Tabbaa; Hakim Tafer; Jason Turner-Maier; Peter Van Heusden; Simon White; Louise Williams; Mark Yandell; Henner Brinkmann; Jean Nicolas Volff; Clifford J. Tabin; Neil Shubin; Manfred Schartl; David B. Jaffe; John H. Postlethwait; Byrappa Venkatesh; Federica Di Palma; Eric S. Lander; Axel Meyer; Kerstin Lindblad-Toh

doi:10.1038/nature12027

The African coelacanth genome provides insights into tetrapod evolution

Chris T. Amemiya, Jessica Alfoldi, Alison P. Lee, Shaohua Fan, Hervé Philippe, Iain MacCallum, Ingo Braasch, Tereza Manousaki, Igor Schneider, Nicolas Rohner, Chris Organ, Domitille Chalopin, Jeramiah J. Smith, Mark Robinson, Rosemary A. Dorrington, Marco Gerdol, Bronwen Aken, Maria Assunta Biscotti, Marco Barucca, Denis BaurainAaron M. Berlin, Gregory L. Blatch, Francesco Buonocore, Thorsten Burmester, Michael S. Campbell, Adriana Canapa, John P. Cannon, Alan Christoffels, Gianluca De Moro, Adrienne L. Edkins, Lin Fan, Anna Maria Fausto, Nathalie Feiner, Mariko Forconi, Junaid Gamieldien, Sante Gnerre, Andreas Gnirke, Jared V. Goldstone, Wilfried Haerty, Mark E. Hahn, Uljana Hesse, Steve Hoffmann, Jeremy Johnson, Sibel I. Karchner, Shigehiro Kuraku, Marcia Lara, Joshua Z. Levin, Gary W. Litman, Evan Mauceli, Tsutomu Miyake, M. Gail Mueller, David R. Nelson, Anne Nitsche, Ettore Olmo, Tatsuya Ota, Alberto Pallavicini, Sumir Panji, Barbara Picone, Chris P. Ponting, Sonja J. Prohaska, Dariusz Przybylski, Nil Ratan Saha, Vydianathan Ravi, Filipe J. Ribeiro, Tatjana Sauka-Spengler, Giuseppe Scapigliati, Stephen M.J. Searle, Ted Sharpe, Oleg Simakov, Peter F. Stadler, John J. Stegeman, Kenta Sumiyama, Diana Tabbaa, Hakim Tafer, Jason Turner-Maier, Peter Van Heusden, Simon White, Louise Williams, Mark Yandell, Henner Brinkmann, Jean Nicolas Volff, Clifford J. Tabin, Neil Shubin, Manfred Schartl, David B. Jaffe, John H. Postlethwait, Byrappa Venkatesh, Federica Di Palma, Eric S. Lander, Axel Meyer, Kerstin Lindblad-Toh

Research output: Contribution to journal › Article › peer-review

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Abstract

The discovery of a living coelacanth specimen in 1938 was remarkable, as this lineage of lobe-finned fish was thought to have become extinct 70 million years ago. The modern coelacanth looks remarkably similar to many of its ancient relatives, and its evolutionary proximity to our own fish ancestors provides a glimpse of the fish that first walked on land. Here we report the genome sequence of the African coelacanth, Latimeria chalumnae. Through a phylogenomic analysis, we conclude that the lungfish, and not the coelacanth, is the closest living relative of tetrapods. Coelacanth protein-coding genes are significantly more slowly evolving than those of tetrapods, unlike other genomic features. Analyses of changes in genes and regulatory elements during the vertebrate adaptation to land highlight genes involved in immunity, nitrogen excretion and the development of fins, tail, ear, eye, brain and olfaction. Functional assays of enhancers involved in the fin-to-limb transition and in the emergence of extra-embryonic tissues show the importance of the coelacanth genome as a blueprint for understanding tetrapod evolution.

Original language	English
Pages (from-to)	311-316
Number of pages	6
Journal	Nature
Volume	496
Issue number	7445
DOIs	https://doi.org/10.1038/nature12027
State	Published - Apr 18 2013

Bibliographical note

Funding Information:
Acknowledgements Acquisition and storage of Latimeria chalumnae samples was supported by grants from the African Coelacanth Ecosystem Programme of the South African National Department of Science and Technology. Generation of the Latimeria chalumnae and Protopterus annectens sequences by the Broad Institute of the Massachusetts Institute of Technology (MIT) and Harvard University was supported by grants from the National Human Genome Research Institute (NHGRI). K.L.T. is the recipient of a EURYI award from the European Science Foundation. We would also like to thank the Genomics Sequencing Platform of the Broad Institute for sequencing the L. chalumnae genome and L. chalumnae and P. annectens transcriptomes, S. Ahamada, R. Stobbs and the Association pour le Protection de Gombesa (APG) for their help in obtaining coelacanth samples, Y. Zhao for the use of data from Rana chensinensis, and L. Gaffney, C. Hamilton and J. Westlund for assistance with figure preparation.

Funding

Acknowledgements Acquisition and storage of Latimeria chalumnae samples was supported by grants from the African Coelacanth Ecosystem Programme of the South African National Department of Science and Technology. Generation of the Latimeria chalumnae and Protopterus annectens sequences by the Broad Institute of the Massachusetts Institute of Technology (MIT) and Harvard University was supported by grants from the National Human Genome Research Institute (NHGRI). K.L.T. is the recipient of a EURYI award from the European Science Foundation. We would also like to thank the Genomics Sequencing Platform of the Broad Institute for sequencing the L. chalumnae genome and L. chalumnae and P. annectens transcriptomes, S. Ahamada, R. Stobbs and the Association pour le Protection de Gombesa (APG) for their help in obtaining coelacanth samples, Y. Zhao for the use of data from Rana chensinensis, and L. Gaffney, C. Hamilton and J. Westlund for assistance with figure preparation.

Funders	Funder number
EUROPEAN SCIENCE FOUNDATION
Eunice Kennedy Shriver National Institute of Child Health and Human Development
Harvard Transdisciplinary Research in Energetics and Cancer Center, Harvard University
Broad Institute of the Massachusetts Institute of Technology
Science and Technology Department of Ningxia
Massachusetts Institute of Technology
Medical Research Council-São Paulo Research Foundation	MC_U137761446
Medical Research Council-São Paulo Research Foundation
Japan Society for the Promotion of Science Fund for the Promotion of Joint International Research	23370101
Japan Society for the Promotion of Science Fund for the Promotion of Joint International Research
Biotechnology and Biological Sciences Research Council	BBS/E/T/000PR6193, BBS/E/T/000PR5885
Biotechnology and Biological Sciences Research Council
National Center for Research Resources	R24RR032670
National Center for Research Resources
National Human Genome Research Institute	R01HG003474, U54HG003067
National Human Genome Research Institute
National Institutes of Health/National Institute of Environmental Health Sciences	R01ES006272, P42ES007381
National Institutes of Health/National Institute of Environmental Health Sciences
NIH National Institute of Child Health and Human Development National Center for Medical Rehabilitation Research	R37HD032443
NIH National Institute of Child Health and Human Development National Center for Medical Rehabilitation Research
NIH Office of the Director	R01OD011116, R24OD011199
NIH Office of the Director

ASJC Scopus subject areas

General

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10.1038/nature12027

Cite this

Amemiya, C. T., Alfoldi, J., Lee, A. P., Fan, S., Philippe, H., MacCallum, I., Braasch, I., Manousaki, T., Schneider, I., Rohner, N., Organ, C., Chalopin, D., Smith, J. J., Robinson, M., Dorrington, R. A., Gerdol, M., Aken, B., Biscotti, M. A., Barucca, M., ... Lindblad-Toh, K. (2013). The African coelacanth genome provides insights into tetrapod evolution. Nature, 496(7445), 311-316. https://doi.org/10.1038/nature12027

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title = "The African coelacanth genome provides insights into tetrapod evolution",

abstract = "The discovery of a living coelacanth specimen in 1938 was remarkable, as this lineage of lobe-finned fish was thought to have become extinct 70 million years ago. The modern coelacanth looks remarkably similar to many of its ancient relatives, and its evolutionary proximity to our own fish ancestors provides a glimpse of the fish that first walked on land. Here we report the genome sequence of the African coelacanth, Latimeria chalumnae. Through a phylogenomic analysis, we conclude that the lungfish, and not the coelacanth, is the closest living relative of tetrapods. Coelacanth protein-coding genes are significantly more slowly evolving than those of tetrapods, unlike other genomic features. Analyses of changes in genes and regulatory elements during the vertebrate adaptation to land highlight genes involved in immunity, nitrogen excretion and the development of fins, tail, ear, eye, brain and olfaction. Functional assays of enhancers involved in the fin-to-limb transition and in the emergence of extra-embryonic tissues show the importance of the coelacanth genome as a blueprint for understanding tetrapod evolution.",

author = "Amemiya, \{Chris T.\} and Jessica Alfoldi and Lee, \{Alison P.\} and Shaohua Fan and Herv{\'e} Philippe and Iain MacCallum and Ingo Braasch and Tereza Manousaki and Igor Schneider and Nicolas Rohner and Chris Organ and Domitille Chalopin and Smith, \{Jeramiah J.\} and Mark Robinson and Dorrington, \{Rosemary A.\} and Marco Gerdol and Bronwen Aken and Biscotti, \{Maria Assunta\} and Marco Barucca and Denis Baurain and Berlin, \{Aaron M.\} and Blatch, \{Gregory L.\} and Francesco Buonocore and Thorsten Burmester and Campbell, \{Michael S.\} and Adriana Canapa and Cannon, \{John P.\} and Alan Christoffels and \{De Moro\}, Gianluca and Edkins, \{Adrienne L.\} and Lin Fan and Fausto, \{Anna Maria\} and Nathalie Feiner and Mariko Forconi and Junaid Gamieldien and Sante Gnerre and Andreas Gnirke and Goldstone, \{Jared V.\} and Wilfried Haerty and Hahn, \{Mark E.\} and Uljana Hesse and Steve Hoffmann and Jeremy Johnson and Karchner, \{Sibel I.\} and Shigehiro Kuraku and Marcia Lara and Levin, \{Joshua Z.\} and Litman, \{Gary W.\} and Evan Mauceli and Tsutomu Miyake and Mueller, \{M. Gail\} and Nelson, \{David R.\} and Anne Nitsche and Ettore Olmo and Tatsuya Ota and Alberto Pallavicini and Sumir Panji and Barbara Picone and Ponting, \{Chris P.\} and Prohaska, \{Sonja J.\} and Dariusz Przybylski and Saha, \{Nil Ratan\} and Vydianathan Ravi and Ribeiro, \{Filipe J.\} and Tatjana Sauka-Spengler and Giuseppe Scapigliati and Searle, \{Stephen M.J.\} and Ted Sharpe and Oleg Simakov and Stadler, \{Peter F.\} and Stegeman, \{John J.\} and Kenta Sumiyama and Diana Tabbaa and Hakim Tafer and Jason Turner-Maier and \{Van Heusden\}, Peter and Simon White and Louise Williams and Mark Yandell and Henner Brinkmann and Volff, \{Jean Nicolas\} and Tabin, \{Clifford J.\} and Neil Shubin and Manfred Schartl and Jaffe, \{David B.\} and Postlethwait, \{John H.\} and Byrappa Venkatesh and \{Di Palma\}, Federica and Lander, \{Eric S.\} and Axel Meyer and Kerstin Lindblad-Toh",

note = "Funding Information: Acknowledgements Acquisition and storage of Latimeria chalumnae samples was supported by grants from the African Coelacanth Ecosystem Programme of the South African National Department of Science and Technology. Generation of the Latimeria chalumnae and Protopterus annectens sequences by the Broad Institute of the Massachusetts Institute of Technology (MIT) and Harvard University was supported by grants from the National Human Genome Research Institute (NHGRI). K.L.T. is the recipient of a EURYI award from the European Science Foundation. We would also like to thank the Genomics Sequencing Platform of the Broad Institute for sequencing the L. chalumnae genome and L. chalumnae and P. annectens transcriptomes, S. Ahamada, R. Stobbs and the Association pour le Protection de Gombesa (APG) for their help in obtaining coelacanth samples, Y. Zhao for the use of data from Rana chensinensis, and L. Gaffney, C. Hamilton and J. Westlund for assistance with figure preparation.",

year = "2013",

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doi = "10.1038/nature12027",

language = "English",

volume = "496",

pages = "311--316",

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Amemiya, CT, Alfoldi, J, Lee, AP, Fan, S, Philippe, H, MacCallum, I, Braasch, I, Manousaki, T, Schneider, I, Rohner, N, Organ, C, Chalopin, D, Smith, JJ, Robinson, M, Dorrington, RA, Gerdol, M, Aken, B, Biscotti, MA, Barucca, M, Baurain, D, Berlin, AM, Blatch, GL, Buonocore, F, Burmester, T, Campbell, MS, Canapa, A, Cannon, JP, Christoffels, A, De Moro, G, Edkins, AL, Fan, L, Fausto, AM, Feiner, N, Forconi, M, Gamieldien, J, Gnerre, S, Gnirke, A, Goldstone, JV, Haerty, W, Hahn, ME, Hesse, U, Hoffmann, S, Johnson, J, Karchner, SI, Kuraku, S, Lara, M, Levin, JZ, Litman, GW, Mauceli, E, Miyake, T, Mueller, MG, Nelson, DR, Nitsche, A, Olmo, E, Ota, T, Pallavicini, A, Panji, S, Picone, B, Ponting, CP, Prohaska, SJ, Przybylski, D, Saha, NR, Ravi, V, Ribeiro, FJ, Sauka-Spengler, T, Scapigliati, G, Searle, SMJ, Sharpe, T, Simakov, O, Stadler, PF, Stegeman, JJ, Sumiyama, K, Tabbaa, D, Tafer, H, Turner-Maier, J, Van Heusden, P, White, S, Williams, L, Yandell, M, Brinkmann, H, Volff, JN, Tabin, CJ, Shubin, N, Schartl, M, Jaffe, DB, Postlethwait, JH, Venkatesh, B, Di Palma, F, Lander, ES, Meyer, A & Lindblad-Toh, K 2013, 'The African coelacanth genome provides insights into tetrapod evolution', Nature, vol. 496, no. 7445, pp. 311-316. https://doi.org/10.1038/nature12027

TY - JOUR

T1 - The African coelacanth genome provides insights into tetrapod evolution

AU - Amemiya, Chris T.

AU - Alfoldi, Jessica

AU - Lee, Alison P.

AU - Fan, Shaohua

AU - Philippe, Hervé

AU - MacCallum, Iain

AU - Braasch, Ingo

AU - Manousaki, Tereza

AU - Schneider, Igor

AU - Rohner, Nicolas

AU - Organ, Chris

AU - Chalopin, Domitille

AU - Smith, Jeramiah J.

AU - Robinson, Mark

AU - Dorrington, Rosemary A.

AU - Gerdol, Marco

AU - Aken, Bronwen

AU - Biscotti, Maria Assunta

AU - Barucca, Marco

AU - Baurain, Denis

AU - Berlin, Aaron M.

AU - Blatch, Gregory L.

AU - Buonocore, Francesco

AU - Burmester, Thorsten

AU - Campbell, Michael S.

AU - Canapa, Adriana

AU - Cannon, John P.

AU - Christoffels, Alan

AU - De Moro, Gianluca

AU - Edkins, Adrienne L.

AU - Fan, Lin

AU - Fausto, Anna Maria

AU - Feiner, Nathalie

AU - Forconi, Mariko

AU - Gamieldien, Junaid

AU - Gnerre, Sante

AU - Gnirke, Andreas

AU - Goldstone, Jared V.

AU - Haerty, Wilfried

AU - Hahn, Mark E.

AU - Hesse, Uljana

AU - Hoffmann, Steve

AU - Johnson, Jeremy

AU - Karchner, Sibel I.

AU - Kuraku, Shigehiro

AU - Lara, Marcia

AU - Levin, Joshua Z.

AU - Litman, Gary W.

AU - Mauceli, Evan

AU - Miyake, Tsutomu

AU - Mueller, M. Gail

AU - Nelson, David R.

AU - Nitsche, Anne

AU - Olmo, Ettore

AU - Ota, Tatsuya

AU - Pallavicini, Alberto

AU - Panji, Sumir

AU - Picone, Barbara

AU - Ponting, Chris P.

AU - Prohaska, Sonja J.

AU - Przybylski, Dariusz

AU - Saha, Nil Ratan

AU - Ravi, Vydianathan

AU - Ribeiro, Filipe J.

AU - Sauka-Spengler, Tatjana

AU - Scapigliati, Giuseppe

AU - Searle, Stephen M.J.

AU - Sharpe, Ted

AU - Simakov, Oleg

AU - Stadler, Peter F.

AU - Stegeman, John J.

AU - Sumiyama, Kenta

AU - Tabbaa, Diana

AU - Tafer, Hakim

AU - Turner-Maier, Jason

AU - Van Heusden, Peter

AU - White, Simon

AU - Williams, Louise

AU - Yandell, Mark

AU - Brinkmann, Henner

AU - Volff, Jean Nicolas

AU - Tabin, Clifford J.

AU - Shubin, Neil

AU - Schartl, Manfred

AU - Jaffe, David B.

AU - Postlethwait, John H.

AU - Venkatesh, Byrappa

AU - Di Palma, Federica

AU - Lander, Eric S.

AU - Meyer, Axel

AU - Lindblad-Toh, Kerstin

N1 - Funding Information: Acknowledgements Acquisition and storage of Latimeria chalumnae samples was supported by grants from the African Coelacanth Ecosystem Programme of the South African National Department of Science and Technology. Generation of the Latimeria chalumnae and Protopterus annectens sequences by the Broad Institute of the Massachusetts Institute of Technology (MIT) and Harvard University was supported by grants from the National Human Genome Research Institute (NHGRI). K.L.T. is the recipient of a EURYI award from the European Science Foundation. We would also like to thank the Genomics Sequencing Platform of the Broad Institute for sequencing the L. chalumnae genome and L. chalumnae and P. annectens transcriptomes, S. Ahamada, R. Stobbs and the Association pour le Protection de Gombesa (APG) for their help in obtaining coelacanth samples, Y. Zhao for the use of data from Rana chensinensis, and L. Gaffney, C. Hamilton and J. Westlund for assistance with figure preparation.

PY - 2013/4/18

Y1 - 2013/4/18

N2 - The discovery of a living coelacanth specimen in 1938 was remarkable, as this lineage of lobe-finned fish was thought to have become extinct 70 million years ago. The modern coelacanth looks remarkably similar to many of its ancient relatives, and its evolutionary proximity to our own fish ancestors provides a glimpse of the fish that first walked on land. Here we report the genome sequence of the African coelacanth, Latimeria chalumnae. Through a phylogenomic analysis, we conclude that the lungfish, and not the coelacanth, is the closest living relative of tetrapods. Coelacanth protein-coding genes are significantly more slowly evolving than those of tetrapods, unlike other genomic features. Analyses of changes in genes and regulatory elements during the vertebrate adaptation to land highlight genes involved in immunity, nitrogen excretion and the development of fins, tail, ear, eye, brain and olfaction. Functional assays of enhancers involved in the fin-to-limb transition and in the emergence of extra-embryonic tissues show the importance of the coelacanth genome as a blueprint for understanding tetrapod evolution.

AB - The discovery of a living coelacanth specimen in 1938 was remarkable, as this lineage of lobe-finned fish was thought to have become extinct 70 million years ago. The modern coelacanth looks remarkably similar to many of its ancient relatives, and its evolutionary proximity to our own fish ancestors provides a glimpse of the fish that first walked on land. Here we report the genome sequence of the African coelacanth, Latimeria chalumnae. Through a phylogenomic analysis, we conclude that the lungfish, and not the coelacanth, is the closest living relative of tetrapods. Coelacanth protein-coding genes are significantly more slowly evolving than those of tetrapods, unlike other genomic features. Analyses of changes in genes and regulatory elements during the vertebrate adaptation to land highlight genes involved in immunity, nitrogen excretion and the development of fins, tail, ear, eye, brain and olfaction. Functional assays of enhancers involved in the fin-to-limb transition and in the emergence of extra-embryonic tissues show the importance of the coelacanth genome as a blueprint for understanding tetrapod evolution.

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UR - http://www.scopus.com/inward/citedby.url?scp=84876271982&partnerID=8YFLogxK

U2 - 10.1038/nature12027

DO - 10.1038/nature12027

M3 - Article

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AN - SCOPUS:84876271982

SN - 0028-0836

VL - 496

SP - 311

EP - 316

JO - Nature

JF - Nature

IS - 7445

ER -

The African coelacanth genome provides insights into tetrapod evolution

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Bibliographical note

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