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The genomic substrate for adaptive radiation in African cichlid fish

Author

Listed:
  • David Brawand

    (Broad Institute of MIT and Harvard
    MRC Functional Genomics Unit, University of Oxford, Oxford OX1 3QX, UK)

  • Catherine E. Wagner

    (Eawag Swiss Federal Institute of Aquatic Science and Technology, Center for Ecology, Evolution & Biogeochemistry, CH-6047 Kastanienbaum, Switzerland
    Institute of Ecology & Evolution, University of Bern, CH-3012 Bern, Switzerland)

  • Yang I. Li

    (MRC Functional Genomics Unit, University of Oxford, Oxford OX1 3QX, UK)

  • Milan Malinsky

    (Gurdon Institute, Cambridge CB2 1QN, UK
    Wellcome Trust Sanger Institute, Hinxton CB10 1SA, 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
    European Molecular Biology Laboratory, 69117 Heidelberg, 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
    Institute of Ecology & Evolution, University of Bern, CH-3012 Bern, 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
    The University of Texas at Austin)

  • Hans A. Hofmann

    (Department of Integrative Biology, Center for Computational Biology and Bioinformatics
    The University of Texas at Austin)

  • 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
    National Cheng Kung University, Tainan City, 704 Taiwan)

  • 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
    Science for Life Laboratory, Uppsala University, 751 23 Uppsala, Sweden)

  • Ole Seehausen

    (Eawag Swiss Federal Institute of Aquatic Science and Technology, Center for Ecology, Evolution & Biogeochemistry, CH-6047 Kastanienbaum, Switzerland
    Institute of Ecology & Evolution, University of Bern, CH-3012 Bern, Switzerland)

  • Federica Di Palma

    (Broad Institute of MIT and Harvard
    Vertebrate and Health Genomics, The Genome Analysis Centre, Norwich NR18 7UH, UK)

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.

Suggested Citation

  • 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, 2014. "The genomic substrate for adaptive radiation in African cichlid fish," Nature, Nature, vol. 513(7518), pages 375-381, September.
  • Handle: RePEc:nat:nature:v:513:y:2014:i:7518:d:10.1038_nature13726
    DOI: 10.1038/nature13726
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    Cited by:

    1. Grégoire Vernaz & Milan Malinsky & Hannes Svardal & Mingliu Du & Alexandra M. Tyers & M. Emília Santos & Richard Durbin & Martin J. Genner & George F. Turner & Eric A. Miska, 2021. "Mapping epigenetic divergence in the massive radiation of Lake Malawi cichlid fishes," Nature Communications, Nature, vol. 12(1), pages 1-13, December.

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