The genomic substrate for adaptive radiation in African cichlid fish

David Brawand, Catherine E. Wagner, Yang I. Li, Milan Malinsky, Irene Keller, Shaohua Fan, Oleg Simakov, Alvin Y. Ng, Zhi Wei Lim, Etienne Bezault, Jason Turner-Maier, Jeremy Johnson, Rosa Alcazar, Hyun Ji Noh, Pamela Russell, Bronwen Aken, Jessica Alföldi, Chris Amemiya, Naoual Azzouzi, Jean François BaroillerFrederique Barloy-Hubler, Aaron Berlin, Ryan Fredric Bloomquist, Karen L. Carleton, Matthew A. Conte, Helena D'Cotta, Orly Eshel, Leslie Gaffney, Francis Galibert, Hugo F. Gante, Sante Gnerre, Lucie Greuter, Richard Guyon, Natalie S. Haddad, Wilfried Haerty, Rayna M. Harris, Hans A. Hofmann, Thibaut Hourlier, Gideon Hulata, David B. Jaffe, Marcia Lara, Alison P. Lee, Iain MacCallum, Salome Mwaiko, Masato Nikaido, Hidenori Nishihara, Catherine Ozouf-Costaz, David J. Penman, Dariusz Przybylski, Michaelle Rakotomanga, Suzy C.P. Renn, Filipe J. Ribeiro, Micha Ron, Walter Salzburger, Luis Sanchez-Pulido, M. Emilia Santos, Steve Searle, Ted Sharpe, Ross Swofford, Frederick J. Tan, Louise Williams, Sarah Young, Shuangye Yin, Norihiro Okada, Thomas D. Kocher, Eric A. Miska, Eric S. Lander, Byrappa Venkatesh, Russell D. Fernald, Axel Meyer, Chris P. Ponting, J. Todd Streelman, Kerstin Lindblad-Toh, Ole Seehausen, Federica Di Palma

Research output: Contribution to journalArticle

400 Citations (Scopus)

Abstract

Cichlid fishes are famous for large, diverse and replicated adaptive radiations in the Great Lakes of East Africa. To understand the molecular mechanisms underlying cichlid phenotypic diversity, we sequenced the genomes and transcriptomes of five lineages of African cichlids: the Nile tilapia (Oreochromis niloticus), an ancestral lineage with low diversity; and four members of the East African lineage: Neolamprologus brichardi/pulcher (older radiation, Lake Tanganyika), Metriaclima zebra (recent radiation, Lake Malawi), Pundamilia nyererei (very recent radiation, Lake Victoria), and Astatotilapia burtoni (riverine species around Lake Tanganyika). We found an excess of gene duplications in the East African lineage compared to tilapia and other teleosts, an abundance of non-coding element divergence, accelerated coding sequence evolution, expression divergence associated with transposable element insertions, and regulation by novel microRNAs. In addition, we analysed sequence data from sixty individuals representing six closely related species from Lake Victoria, and show genome-wide diversifying selection on coding and regulatory variants, some of which were recruited from ancient polymorphisms. We conclude that a number of molecular mechanisms shaped East African cichlid genomes, and that amassing of standing variation during periods of relaxed purifying selection may have been important in facilitating subsequent evolutionary diversification.

Original languageEnglish (US)
Pages (from-to)375-381
Number of pages7
JournalNature
Volume513
Issue number7518
DOIs
StatePublished - Oct 2 2015

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Cichlids
Lakes
Radiation
Tanzania
Victoria
Genome
Tilapia
Malawi
Eastern Africa
DNA Transposable Elements
Gene Duplication
Equidae
MicroRNAs
Transcriptome

ASJC Scopus subject areas

  • General

Cite this

Brawand, D., Wagner, C. E., Li, Y. I., Malinsky, M., Keller, I., Fan, S., ... Di Palma, F. (2015). The genomic substrate for adaptive radiation in African cichlid fish. Nature, 513(7518), 375-381. https://doi.org/10.1038/nature13726

The genomic substrate for adaptive radiation in African cichlid fish. / Brawand, David; Wagner, Catherine E.; Li, Yang I.; Malinsky, Milan; Keller, Irene; Fan, Shaohua; Simakov, Oleg; Ng, Alvin Y.; Lim, Zhi Wei; Bezault, Etienne; Turner-Maier, Jason; Johnson, Jeremy; Alcazar, Rosa; Noh, Hyun Ji; Russell, Pamela; Aken, Bronwen; Alföldi, Jessica; Amemiya, Chris; Azzouzi, Naoual; Baroiller, Jean François; Barloy-Hubler, Frederique; Berlin, Aaron; Bloomquist, Ryan Fredric; Carleton, Karen L.; Conte, Matthew A.; D'Cotta, Helena; Eshel, Orly; Gaffney, Leslie; Galibert, Francis; Gante, Hugo F.; Gnerre, Sante; Greuter, Lucie; Guyon, Richard; Haddad, Natalie S.; Haerty, Wilfried; Harris, Rayna M.; Hofmann, Hans A.; Hourlier, Thibaut; Hulata, Gideon; Jaffe, David B.; Lara, Marcia; Lee, Alison P.; MacCallum, Iain; Mwaiko, Salome; Nikaido, Masato; Nishihara, Hidenori; Ozouf-Costaz, Catherine; Penman, David J.; Przybylski, Dariusz; Rakotomanga, Michaelle; Renn, Suzy C.P.; Ribeiro, Filipe J.; Ron, Micha; Salzburger, Walter; Sanchez-Pulido, Luis; Santos, M. Emilia; Searle, Steve; Sharpe, Ted; Swofford, Ross; Tan, Frederick J.; Williams, Louise; Young, Sarah; Yin, Shuangye; Okada, Norihiro; Kocher, Thomas D.; Miska, Eric A.; Lander, Eric S.; Venkatesh, Byrappa; Fernald, Russell D.; Meyer, Axel; Ponting, Chris P.; Streelman, J. Todd; Lindblad-Toh, Kerstin; Seehausen, Ole; Di Palma, Federica.

In: Nature, Vol. 513, No. 7518, 02.10.2015, p. 375-381.

Research output: Contribution to journalArticle

Brawand, D, Wagner, CE, Li, YI, Malinsky, M, Keller, I, Fan, S, Simakov, O, Ng, AY, Lim, ZW, Bezault, E, Turner-Maier, J, Johnson, J, Alcazar, R, Noh, HJ, Russell, P, Aken, B, Alföldi, J, Amemiya, C, Azzouzi, N, Baroiller, JF, Barloy-Hubler, F, Berlin, A, Bloomquist, RF, Carleton, KL, Conte, MA, D'Cotta, H, Eshel, O, Gaffney, L, Galibert, F, Gante, HF, Gnerre, S, Greuter, L, Guyon, R, Haddad, NS, Haerty, W, Harris, RM, Hofmann, HA, Hourlier, T, Hulata, G, Jaffe, DB, Lara, M, Lee, AP, MacCallum, I, Mwaiko, S, Nikaido, M, Nishihara, H, Ozouf-Costaz, C, Penman, DJ, Przybylski, D, Rakotomanga, M, Renn, SCP, Ribeiro, FJ, Ron, M, Salzburger, W, Sanchez-Pulido, L, Santos, ME, Searle, S, Sharpe, T, Swofford, R, Tan, FJ, Williams, L, Young, S, Yin, S, Okada, N, Kocher, TD, Miska, EA, Lander, ES, Venkatesh, B, Fernald, RD, Meyer, A, Ponting, CP, Streelman, JT, Lindblad-Toh, K, Seehausen, O & Di Palma, F 2015, 'The genomic substrate for adaptive radiation in African cichlid fish', Nature, vol. 513, no. 7518, pp. 375-381. https://doi.org/10.1038/nature13726
Brawand D, Wagner CE, Li YI, Malinsky M, Keller I, Fan S et al. The genomic substrate for adaptive radiation in African cichlid fish. Nature. 2015 Oct 2;513(7518):375-381. https://doi.org/10.1038/nature13726
Brawand, David ; Wagner, Catherine E. ; Li, Yang I. ; Malinsky, Milan ; Keller, Irene ; Fan, Shaohua ; Simakov, Oleg ; Ng, Alvin Y. ; Lim, Zhi Wei ; Bezault, Etienne ; Turner-Maier, Jason ; Johnson, Jeremy ; Alcazar, Rosa ; Noh, Hyun Ji ; Russell, Pamela ; Aken, Bronwen ; Alföldi, Jessica ; Amemiya, Chris ; Azzouzi, Naoual ; Baroiller, Jean François ; Barloy-Hubler, Frederique ; Berlin, Aaron ; Bloomquist, Ryan Fredric ; Carleton, Karen L. ; Conte, Matthew A. ; D'Cotta, Helena ; Eshel, Orly ; Gaffney, Leslie ; Galibert, Francis ; Gante, Hugo F. ; Gnerre, Sante ; Greuter, Lucie ; Guyon, Richard ; Haddad, Natalie S. ; Haerty, Wilfried ; Harris, Rayna M. ; Hofmann, Hans A. ; Hourlier, Thibaut ; Hulata, Gideon ; Jaffe, David B. ; Lara, Marcia ; Lee, Alison P. ; MacCallum, Iain ; Mwaiko, Salome ; Nikaido, Masato ; Nishihara, Hidenori ; Ozouf-Costaz, Catherine ; Penman, David J. ; Przybylski, Dariusz ; Rakotomanga, Michaelle ; Renn, Suzy C.P. ; Ribeiro, Filipe J. ; Ron, Micha ; Salzburger, Walter ; Sanchez-Pulido, Luis ; Santos, M. Emilia ; Searle, Steve ; Sharpe, Ted ; Swofford, Ross ; Tan, Frederick J. ; Williams, Louise ; Young, Sarah ; Yin, Shuangye ; Okada, Norihiro ; Kocher, Thomas D. ; Miska, Eric A. ; Lander, Eric S. ; Venkatesh, Byrappa ; Fernald, Russell D. ; Meyer, Axel ; Ponting, Chris P. ; Streelman, J. Todd ; Lindblad-Toh, Kerstin ; Seehausen, Ole ; Di Palma, Federica. / The genomic substrate for adaptive radiation in African cichlid fish. In: Nature. 2015 ; Vol. 513, No. 7518. pp. 375-381.
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abstract = "Cichlid fishes are famous for large, diverse and replicated adaptive radiations in the Great Lakes of East Africa. To understand the molecular mechanisms underlying cichlid phenotypic diversity, we sequenced the genomes and transcriptomes of five lineages of African cichlids: the Nile tilapia (Oreochromis niloticus), an ancestral lineage with low diversity; and four members of the East African lineage: Neolamprologus brichardi/pulcher (older radiation, Lake Tanganyika), Metriaclima zebra (recent radiation, Lake Malawi), Pundamilia nyererei (very recent radiation, Lake Victoria), and Astatotilapia burtoni (riverine species around Lake Tanganyika). We found an excess of gene duplications in the East African lineage compared to tilapia and other teleosts, an abundance of non-coding element divergence, accelerated coding sequence evolution, expression divergence associated with transposable element insertions, and regulation by novel microRNAs. In addition, we analysed sequence data from sixty individuals representing six closely related species from Lake Victoria, and show genome-wide diversifying selection on coding and regulatory variants, some of which were recruited from ancient polymorphisms. We conclude that a number of molecular mechanisms shaped East African cichlid genomes, and that amassing of standing variation during periods of relaxed purifying selection may have been important in facilitating subsequent evolutionary diversification.",
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AU - Brawand, David

AU - Wagner, Catherine E.

AU - Li, Yang I.

AU - Malinsky, Milan

AU - Keller, Irene

AU - Fan, Shaohua

AU - Simakov, Oleg

AU - Ng, Alvin Y.

AU - Lim, Zhi Wei

AU - Bezault, Etienne

AU - Turner-Maier, Jason

AU - Johnson, Jeremy

AU - Alcazar, Rosa

AU - Noh, Hyun Ji

AU - Russell, Pamela

AU - Aken, Bronwen

AU - Alföldi, Jessica

AU - Amemiya, Chris

AU - Azzouzi, Naoual

AU - Baroiller, Jean François

AU - Barloy-Hubler, Frederique

AU - Berlin, Aaron

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AU - Carleton, Karen L.

AU - Conte, Matthew A.

AU - D'Cotta, Helena

AU - Eshel, Orly

AU - Gaffney, Leslie

AU - Galibert, Francis

AU - Gante, Hugo F.

AU - Gnerre, Sante

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AU - Haddad, Natalie S.

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AU - Hofmann, Hans A.

AU - Hourlier, Thibaut

AU - Hulata, Gideon

AU - Jaffe, David B.

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AU - Lee, Alison P.

AU - MacCallum, Iain

AU - Mwaiko, Salome

AU - Nikaido, Masato

AU - Nishihara, Hidenori

AU - Ozouf-Costaz, Catherine

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AU - Przybylski, Dariusz

AU - Rakotomanga, Michaelle

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AU - Ron, Micha

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AU - Sanchez-Pulido, Luis

AU - Santos, M. Emilia

AU - Searle, Steve

AU - Sharpe, Ted

AU - Swofford, Ross

AU - Tan, Frederick J.

AU - Williams, Louise

AU - Young, Sarah

AU - Yin, Shuangye

AU - Okada, Norihiro

AU - Kocher, Thomas D.

AU - Miska, Eric A.

AU - Lander, Eric S.

AU - Venkatesh, Byrappa

AU - Fernald, Russell D.

AU - Meyer, Axel

AU - Ponting, Chris P.

AU - Streelman, J. Todd

AU - Lindblad-Toh, Kerstin

AU - Seehausen, Ole

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AB - Cichlid fishes are famous for large, diverse and replicated adaptive radiations in the Great Lakes of East Africa. To understand the molecular mechanisms underlying cichlid phenotypic diversity, we sequenced the genomes and transcriptomes of five lineages of African cichlids: the Nile tilapia (Oreochromis niloticus), an ancestral lineage with low diversity; and four members of the East African lineage: Neolamprologus brichardi/pulcher (older radiation, Lake Tanganyika), Metriaclima zebra (recent radiation, Lake Malawi), Pundamilia nyererei (very recent radiation, Lake Victoria), and Astatotilapia burtoni (riverine species around Lake Tanganyika). We found an excess of gene duplications in the East African lineage compared to tilapia and other teleosts, an abundance of non-coding element divergence, accelerated coding sequence evolution, expression divergence associated with transposable element insertions, and regulation by novel microRNAs. In addition, we analysed sequence data from sixty individuals representing six closely related species from Lake Victoria, and show genome-wide diversifying selection on coding and regulatory variants, some of which were recruited from ancient polymorphisms. We conclude that a number of molecular mechanisms shaped East African cichlid genomes, and that amassing of standing variation during periods of relaxed purifying selection may have been important in facilitating subsequent evolutionary diversification.

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