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 Baroiller, Frederique Barloy-Hubler, Aaron Berlin, Ryan 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 () and Federica Di Palma ()
Additional contact information
David Brawand: Broad Institute of MIT and Harvard
Catherine E. Wagner: Eawag Swiss Federal Institute of Aquatic Science and Technology, Center for Ecology, Evolution & Biogeochemistry, CH-6047 Kastanienbaum, Switzerland
Yang I. Li: MRC Functional Genomics Unit, University of Oxford, Oxford OX1 3QX, UK
Milan Malinsky: Gurdon Institute, Cambridge CB2 1QN, UK
Irene Keller: Institute of Ecology & Evolution, University of Bern, CH-3012 Bern, Switzerland
Shaohua Fan: University of Konstanz, D-78457 Konstanz, Germany
Oleg Simakov: University of Konstanz, D-78457 Konstanz, Germany
Alvin Y. Ng: Institute of Molecular and Cell Biology, A*STAR, 138673 Singapore
Zhi Wei Lim: Institute of Molecular and Cell Biology, A*STAR, 138673 Singapore
Etienne Bezault: Reed College
Jason Turner-Maier: Broad Institute of MIT and Harvard
Jeremy Johnson: Broad Institute of MIT and Harvard
Rosa Alcazar: Stanford University
Hyun Ji Noh: Broad Institute of MIT and Harvard
Pamela Russell: California Institute of Technology
Bronwen Aken: Wellcome Trust Sanger Institute, Hinxton CB10 1SA, UK
Jessica Alföldi: Broad Institute of MIT and Harvard
Chris Amemiya: Benaroya Research Institute at Virginia Mason
Naoual Azzouzi: Institut Génétique et Développement, CNRS/University of Rennes, 35043 Rennes, France
Jean-François Baroiller: CIRAD, Campus International de Baillarguet, TA B-110/A, 34398 Montpellier cedex 5, France
Frederique Barloy-Hubler: Institut Génétique et Développement, CNRS/University of Rennes, 35043 Rennes, France
Aaron Berlin: Broad Institute of MIT and Harvard
Ryan Bloomquist: School of Biology, Georgia Institute of Technology
Karen L. Carleton: University of Maryland, College Park
Matthew A. Conte: University of Maryland, College Park
Helena D'Cotta: CIRAD, Campus International de Baillarguet, TA B-110/A, 34398 Montpellier cedex 5, France
Orly Eshel: Animal Genetics, Institute of Animal Science, ARO, The Volcani Center, Bet-Dagan, 50250 Israel
Leslie Gaffney: Broad Institute of MIT and Harvard
Francis Galibert: Institut Génétique et Développement, CNRS/University of Rennes, 35043 Rennes, France
Hugo F. Gante: Zoological Institute, University of Basel, CH-4051 Basel, Switzerland
Sante Gnerre: Broad Institute of MIT and Harvard
Lucie Greuter: Eawag Swiss Federal Institute of Aquatic Science and Technology, Center for Ecology, Evolution & Biogeochemistry, CH-6047 Kastanienbaum, Switzerland
Richard Guyon: Institut Génétique et Développement, CNRS/University of Rennes, 35043 Rennes, France
Natalie S. Haddad: School of Biology, Georgia Institute of Technology
Wilfried Haerty: MRC Functional Genomics Unit, University of Oxford, Oxford OX1 3QX, UK
Rayna M. Harris: Department of Integrative Biology, Center for Computational Biology and Bioinformatics
Hans A. Hofmann: Department of Integrative Biology, Center for Computational Biology and Bioinformatics
Thibaut Hourlier: Wellcome Trust Sanger Institute, Hinxton CB10 1SA, UK
Gideon Hulata: Animal Genetics, Institute of Animal Science, ARO, The Volcani Center, Bet-Dagan, 50250 Israel
David B. Jaffe: Broad Institute of MIT and Harvard
Marcia Lara: Broad Institute of MIT and Harvard
Alison P. Lee: Institute of Molecular and Cell Biology, A*STAR, 138673 Singapore
Iain MacCallum: Broad Institute of MIT and Harvard
Salome Mwaiko: Eawag Swiss Federal Institute of Aquatic Science and Technology, Center for Ecology, Evolution & Biogeochemistry, CH-6047 Kastanienbaum, Switzerland
Masato Nikaido: Tokyo Institute of Technology, Tokyo, 226-8501 Yokohama, Japan
Hidenori Nishihara: Tokyo Institute of Technology, Tokyo, 226-8501 Yokohama, Japan
Catherine Ozouf-Costaz: Systématique, Adaptation, Evolution, National Museum of Natural History, 75005 Paris, France
David J. Penman: Institute of Aquaculture, University of Stirling, Stirling FK9 4LA, UK
Dariusz Przybylski: Broad Institute of MIT and Harvard
Michaelle Rakotomanga: Institut Génétique et Développement, CNRS/University of Rennes, 35043 Rennes, France
Suzy C. P. Renn: Reed College
Filipe J. Ribeiro: Broad Institute of MIT and Harvard
Micha Ron: Animal Genetics, Institute of Animal Science, ARO, The Volcani Center, Bet-Dagan, 50250 Israel
Walter Salzburger: Zoological Institute, University of Basel, CH-4051 Basel, Switzerland
Luis Sanchez-Pulido: MRC Functional Genomics Unit, University of Oxford, Oxford OX1 3QX, UK
M. Emilia Santos: Zoological Institute, University of Basel, CH-4051 Basel, Switzerland
Steve Searle: Wellcome Trust Sanger Institute, Hinxton CB10 1SA, UK
Ted Sharpe: Broad Institute of MIT and Harvard
Ross Swofford: Broad Institute of MIT and Harvard
Frederick J. Tan: Carnegie Institution of Washington
Louise Williams: Broad Institute of MIT and Harvard
Sarah Young: Broad Institute of MIT and Harvard
Shuangye Yin: Broad Institute of MIT and Harvard
Norihiro Okada: Tokyo Institute of Technology, Tokyo, 226-8501 Yokohama, Japan
Thomas D. Kocher: University of Maryland, College Park
Eric A. Miska: Gurdon Institute, Cambridge CB2 1QN, UK
Eric S. Lander: Broad Institute of MIT and Harvard
Byrappa Venkatesh: Institute of Molecular and Cell Biology, A*STAR, 138673 Singapore
Russell D. Fernald: Stanford University
Axel Meyer: University of Konstanz, D-78457 Konstanz, Germany
Chris P. Ponting: MRC Functional Genomics Unit, University of Oxford, Oxford OX1 3QX, UK
J. Todd Streelman: School of Biology, Georgia Institute of Technology
Kerstin Lindblad-Toh: Broad Institute of MIT and Harvard
Ole Seehausen: Eawag Swiss Federal Institute of Aquatic Science and Technology, Center for Ecology, Evolution & Biogeochemistry, CH-6047 Kastanienbaum, Switzerland
Federica Di Palma: Broad Institute of MIT and Harvard

Nature, 2014, vol. 513, issue 7518, 375-381

Abstract: 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.

Date: 2014
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DOI: 10.1038/nature13726

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