Evolution of genes and genomes on the : Drosophila: phylogeny : Abstract : Nature

Nature 450, 203-218 (8 November 2007) | doi:10.1038/nature06341; Received 19 July 2007; Accepted 5 October 2007

Evolution of genes and genomes on the Drosophila phylogeny

Drosophila 12 Genomes Consortium

Department of Molecular Biology and Genetics, Cornell University, Ithaca, New York 14853, USA.
Life Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94720, USA.
Center for Integrative Genomics, Department of Molecular and Cell Biology, University of California at Berkeley, Berkeley, California 94720, USA.
Agencourt Bioscience Corporation, Beverly, Massachusetts 01915, USA.
Faculty of Life Sciences, University of Manchester, Manchester M13 9PT, UK.
Laboratory of Cellular and Developmental Biology, National Institutes of Health, Bethesda, Maryland 20892, USA.
Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona 85721, USA.
Department of Biology, Indiana University, Bloomington, Indiana 47405, USA.
Computer Science and Artificial Intelligence Laboratory, Cambridge, Massachusetts 02139, USA.
Broad Institute of MIT and Harvard, 7 Cambridge Center, Cambridge, Massachusetts 02142, USA.
Department of Molecular and Cellular Biology, Harvard University, Cambridge, Massachusetts 02138, USA.
FlyBase, The Biological Laboratories, Harvard University, Cambridge, Massachusetts 02138, USA.
Department of Molecular and Cell Biology, University of California at Berkeley, Berkeley, California 94720, USA.
Biophysics Graduate Group, University of California at Berkeley, Berkeley, California 94720, USA.
Field of Ecology and Evolutionary Biology, Cornell University, Ithaca, New York 14853, USA.
Centro de Biología Molecular Severo Ochoa, Universidad Autónoma de Madrid, Madrid 28049, Spain.
Department of Ecology and Evolutionary Biology, Brown University, Providence, Rhode Island 02912, USA.
Structural Studies Division, MRC Laboratory of Molecular Biology, Cambridge CB2 2QH, UK.
Departament de Genètica, Universitat de Barcelona, Barcelona 08071, Spain.
Department of Biology, Pennsylvania State University, University Park, Pennsylvania 16802, USA.
Department of Genetics, University of Georgia, Athens, Georgia 30602, USA.
Linnaeus Centre for Bioinformatics, Uppsala Universitet, Uppsala, SE-75124, Sweden.
Department of Ecology and Evolution, University of Chicago, Chicago, Illinois 60637, USA.
Department of Biology, McMaster University, Hamilton, Ontario, L8S 4K1, Canada.
School of Biology, University of St. Andrews, Fife KY16 9TH, UK.
Dipartimento di Genetica e Microbiologia dell'Università di Bari, Bari, 70126, Italy.
Department of Genetics, University of Melbourne, Melbourne 3010, Australia.
Computer Science Department, Stanford University, Stanford, California 94305, USA.
Section of Evolution and Ecology and Center for Population Biology, University of California at Davis, Davis, California 95616, USA.
BioMolecular Engineering Research Center, Boston University, Boston, Massachusetts 02215, USA.
Research Group in Biomedical Informatics, Institut Municipal d'Investigacio Medica, Universitat Pompeu Fabra, Barcelona 08003, Catalonia, Spain.
Department of Bioengineering, University of California at Berkeley, Berkeley, California 94720, USA.
Laboratory for Computational Genomics, Washington University, St Louis, Missouri 63108, USA.
Animal and Plant Sciences, The University of Sheffield, Sheffield S10 2TN, UK.
Department of Biology, Syracuse University, Syracuse, New York 13244, USA.
Departamento de Genética, Universidade Federal do Rio de Janeiro, Rio de Janeiro 21944-970, Brazil.
Tucson Stock Center, Tucson, Arizona 85721, USA.
Department of Mathematics, University of California at Berkeley, Berkeley, California 94720, USA.
Genome Center, University of California at Davis, Davis, California 95616, USA.
Genome Sequencing Center, Washington University School of Medicine, St Louis, Missouri 63108, USA.
Department of Biology, University of Winnipeg, Winnipeg, Manitoba R3B 2E9, Canada.
Department of Biological Sciences, University of Iowa, Iowa City, Iowa 52242, USA.
School of Informatics, Indiana University, Bloomington, Indiana 47405, USA.
Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SA, UK.
Center for Bioinformatics and Computational Biology, University of Maryland, College Park, Maryland 20742, USA.
Department of Biological Sciences, Illinois State University, Normal, Illinois 61790, USA.
Department of Biology, University of Rochester, Rochester, New York 14627, USA.
Bee Research Lab, USDA-ARS, Beltsville, Maryland 20705, USA.
Center for Evolutionary Functional Genomics, Biodesign Institute, Arizona State University, Tempe, Arizona 85287, USA.
Department of Computer Science, University of Leipzig, Leipzig 04107, Germany.
Departamento de Genética, Universidade Federal do Rio Grande do Sul, Porto Alegre/RS 68011, Brazil.
Department of Biology, Duke University, Durham, New Carolina 27708, USA.
Department of Genetics, North Carolina State University, Raleigh, North Caroline 27695, USA.
Health Center, University of Connecticut, Farmington, Connecticut 06030, USA.
Center of Genomic Regulation, Barcelona 8003, Catalonia, Spain.
Institute of Evolutionary Biology, University of Edinburgh, Edinburgh EH9 3JT, UK.
J. Craig Venter Institute, Rockville, Maryland 20850, USA.
MRC Functional Genetics Unit, University of Oxford, Oxford OX1 3QX, UK.
Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford OX1 3QX, UK.
Center for Biomolecular Science and Engineering, University of California at Santa Cruz, Santa Cruz, California 95064, USA.
Department of Human Genetics, University of Chicago, Chicago, Illinois 60637, USA.
Umeå Center for Molecular Pathogenesis, Umeå University, Umeå SE-90187, Sweden.
Department of Biology and Carolina Center for Genome Sciences, The University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27599, USA.
Institute of Zoology, Regent's Park, London NW1 4RY, UK.
Drosophila Heterochromatin Genome Project, Department of Genome and Computational Biology, Lawrence Berkeley National Laboratory, Berkeley, California 94720, USA.
Kyorin University, School of Medicine, Mitaka, Tokyo 181-8611, Japan.
Department of Biochemistry and Molecular Biology, University of Southern Denmark, Odense M DK-5230, Denmark
Arizona Genomics Institute, Department of Plant Sciences and BIO5, University of Arizona, Tucson, Arizona 85721, USA.
Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts 02138, USA.
School of Life Sciences, Arizona State University, Tempe, Arizona 85287, USA.
Department of Environmental Science, Policy and Management, University of California at Berkeley, Berkeley, California 94720, USA.
Department of Entomology, Cornell University, Ithaca, New York 14853, USA.
Beijing Genomics Institute at ShenZhen, ShenZhen 518083, China.
Departament Genètica i Microbiologia, Universitat Autònoma de Barcelona, Bellaterra 08193, Spain.
Department of Cell Biology and Molecular Genetics, University of Maryland, College Park, Maryland 20742, USA.
Janelia Farm Research Campus, Howard Hughes Medical Institue, Ashburn, Viginia 20147-2408, USA.
Department of Zoology, University of Cambridge, Cambridge, CB2 3EJ, UK.
Institue of Biology, University of Copenhagen, DK-2100 Copenhagen Ø, Denmark.
Bioinformatics Centre, Department of Molecular Biology, University of Copenhagen, DK-2200 Copenhagen N, Denmark.
Dipartimento di Biochimica e Biologia Molecolare, Università di Bari and Istituto Tecnologie Biomediche del Consiglio Nazionale delle Ricerche, Bari 70126, Italy.
Department of Ecology and Evolutionary Biology, Yale University, New Haven, Connecticut 06520, USA.
Department of Biomedical Informatics, Arizona State University, Tempe, Arizona 85287, USA.
National Center for Biotechnology Information, National Institutes of Health, Bethesda, Maryland 20894, USA.
Bioinformatics and Genomics Laboratory, Institut Jacques Monod, Paris, 75251, France.
Department of Molecular Biology, Cell Biology and Biochemistry, Brown University, Providence, Rhode Island 02912, USA.
Departamento de Genética, Centro de Ciências Biológicas, Universidade Federal de Pernambuco, Recife/PE 68011, Brazil.
Centro Acadêmico de Vitória, Universidade Federal de Pernambuco, Vitória de Santo Antão/PE, Brazil.
Cajal Institute, CSIC, Madrid 28002, Spain.
Department of Biology, Emory University, Atlanta, Georgia 30322, USA.
Department of Biological Sciences, Carnegie Mellon University, Pittsburgh, Pennsylvania 15213, USA.
Biomedical Informatics, Stanford University, Stanford, California 94305, USA.
Department of Biology, San Francisco State University, San Francisco, California 94132, USA.
Department of Biology, University of Munich, 82152 Planegg-Martinsried, Germany.
Institute of Evolutionary Biology, Setagaya-ku, Tokyo 158-0098, Japan.
Shiba Gakuen, Minato-ku, Tokyo 105-0011, Japan.
European Bioinformatics Institute, Hinxton, CB10 1SD, UK.
Department of Biology, City University of New York at Queens, Flushing, New York 11367, USA.
Department of Biological Sciences and Department of Medicine, University of Alberta, Edmonton, Alberta T6G 2E9, Canada.
Department of Developmental Biology and Neurosciences, Tohoku University, Sendai 980-8578, Japan.
Institute for Physical Science and Technology, University of Maryland, College Park, Maryland 20742, USA.
Hokkaido University, EESBIO, Sapporo, Hokkaido 060-0810, Japan.
Faculty of Medecine, Universite de Geneve, Geneva CH-1211, Switzerland.
A list of participants and affiliations appears at the end of the paper.

Correspondence to: Correspondence and requests for materials should be addressed to A.G.C. (Email: ac347@cornell.edu), M.B.E. (Email: mbeisen@lbl.gov), D.R.S. (Email: douglas.smith@agencourt.com), C.M.B. (Email: casey.bergman@manchester.ac.uk), W.G. (Email: gelbart@morgan.harvard.edu), B.O. (Email: oliver@helix.nih.gov), T.A.M. (Email: tmarkow@public.arl.arizona.edu), T.C.K. (Email: kaufman@indiana.edu), M.K. (Email: manoli@mit.edu), V.N.I. (Email: venky@berkeley.edu), T.B.S. (Email: tbs7@cornell.edu), A.M.L. (Email: aml69@cornell.edu), D.A.P. (Email: danielapollard@alum.bowdoin.edu), N.D.S. (Email: nds25@cornell.edu), or collectively to Email: 12flies@morgan.harvard.edu.

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Comparative analysis of multiple genomes in a phylogenetic framework dramatically improves the precision and sensitivity of evolutionary inference, producing more robust results than single-genome analyses can provide. The genomes of 12 Drosophila species, ten of which are presented here for the first time (sechellia, simulans, yakuba, erecta, ananassae, persimilis, willistoni, mojavensis, virilis and grimshawi), illustrate how rates and patterns of sequence divergence across taxa can illuminate evolutionary processes on a genomic scale. These genome sequences augment the formidable genetic tools that have made Drosophila melanogaster a pre-eminent model for animal genetics, and will further catalyse fundamental research on mechanisms of development, cell biology, genetics, disease, neurobiology, behaviour, physiology and evolution. Despite remarkable similarities among these Drosophila species, we identified many putatively non-neutral changes in protein-coding genes, non-coding RNA genes, and cis-regulatory regions. These may prove to underlie differences in the ecology and behaviour of these diverse species.

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