Letter

Genetic diversity of the African malaria vector Anopheles gambiae

Received:
Accepted:
Published online:

Abstract

The sustainability of malaria control in Africa is threatened by the rise of insecticide resistance in Anopheles mosquitoes, which transmit the disease1. To gain a deeper understanding of how mosquito populations are evolving, here we sequenced the genomes of 765 specimens of Anopheles gambiae and Anopheles coluzzii sampled from 15 locations across Africa, and identified over 50 million single nucleotide polymorphisms within the accessible genome. These data revealed complex population structure and patterns of gene flow, with evidence of ancient expansions, recent bottlenecks, and local variation in effective population size. Strong signals of recent selection were observed in insecticide-resistance genes, with several sweeps spreading over large geographical distances and between species. The design of new tools for mosquito control using gene-drive systems will need to take account of high levels of genetic diversity in natural mosquito populations.

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European Nucleotide Archive

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Acknowledgements

The authors would like to thank the staff of the Wellcome Trust Sanger Institute Sample Logistics, Sequencing and Informatics facilities for their contributions. This work was supported by the Wellcome Trust (090770/Z/09/Z; 090532/Z/09/Z; 098051) and Medical Research Council UK and the Department for International Development (DFID) (MR/M006212/1). M.K.N.L. was supported by MRC grant G1100339. S.O.’L. and A.B. were supported by a grant from the Foundation for the National Institutes of Health through the Vector-Based Control of Transmission: Discovery Research (VCTR) program of the Grand Challenges in Global Health initiative of the Bill & Melinda Gates Foundation. D.W., C.S.W., H.D.M. and M.J.D. were supported by Award Numbers U19AI089674 and R01AI082734 from the National Institute of Allergy and Infectious Diseases (NIAID). The content is solely the responsibility of the authors and does not necessarily represent the official views of the NIAID or NIH. T.A. was supported by a Sir Henry Wellcome Postdoctoral Fellowship.

Author information

Affiliations

  1. Malaria Programme, Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, UK

    • Alistair Miles
    • , Chris S. Clarkson
    • , Krzysztof Kozak
    • , Richard D. Pearson
    • , Martin J. Donnelly
    • , Mara K. N. Lawniczak
    • , Dominic P. Kwiatkowski
    • , Jim Stalker
    • , Eleanor Drury
    • , Daniel Mead
    • , Dushyanth Jyothi
    • , Cinzia Malangone
    •  & Rachel Giacomantonio
  2. MRC Centre for Genomics and Global Health, University of Oxford, Oxford OX3 7BN, UK

    • Alistair Miles
    • , Nicholas J. Harding
    • , Giordano Bottà
    • , Tiago Antão
    • , Richard D. Pearson
    • , Dominic P. Kwiatkowski
    • , Kirk Rockett
    • , Anna Jeffreys
    • , Christina Hubbart
    • , Kate Rowlands
    • , Paul Vauterin
    • , Ben Jeffery
    • , Ian Wright
    • , Lee Hart
    • , Krzysztof Kluczyński
    • , Victoria Cornelius
    •  & Christa Henrichs
  3. Istituto Pasteur Italia – Fondazione Cenci Bolognetti, Dipartimento di Sanita Pubblica e Malattie Infettive, Università di Roma SAPIENZA, Rome, Italy

    • Giordano Bottà
    • , Beniamino Caputo
    •  & Alessandra della Torre
  4. Department of Vector Biology, Liverpool School of Tropical Medicine, Pembroke Place, Liverpool L3 5QA, UK

    • Chris S. Clarkson
    • , Tiago Antão
    • , Martin J. Donnelly
    • , David Weetman
    • , Craig S. Wilding
    •  & Alison T. Isaacs
  5. University of Montana, Missoula, Montana 59812, USA

    • Tiago Antão
  6. Department of Genetics, Rutgers University, 604 Alison Road, Piscataway, New Jersey 08854, USA

    • Daniel R. Schrider
    •  & Andrew D. Kern
  7. Genome Sequencing and Analysis Program, Broad Institute, 415 Main Street, Cambridge, Maryland 02142, USA

    • Seth Redmond
    •  & Daniel E. Neafsey
  8. Department of Entomology, Virginia Tech, Blacksburg, Virginia 24061, USA

    • Igor Sharakhov
  9. Laboratory of Ecology, Genetics and Environmental Protection, Tomsk State University, Tomsk 634050, Russia

    • Igor Sharakhov
  10. Eck Institute for Global Health, Department of Biological Sciences, University of Notre Dame, Indiana 46556, USA

    • Christina Bergey
    • , Nora J. Besansky
    •  & Kyanne R. Rohatgi
  11. Groningen Institute for Evolutionary Life Sciences (GELIFES), Nijenborgh 7, 9747 AG Groningen, The Netherlands

    • Michael C. Fontaine
  12. Unité d’Ecologie des Systèmes Vectoriels, Centre International de Recherches Médicales de Franceville, Franceville, Gabon

    • Diego Ayala
    •  & Nohal Elissa
  13. Institut de Recherche pour le Développement (IRD), UMR MIVEGEC (UM1, UM2, CNRS 5290, IRD 224), Montpellier, France

    • Diego Ayala
    •  & Carlo Costantini
  14. Department of Life Sciences, Imperial College, Silwood Park, Ascot, Berkshire SL5 7PY, UK

    • Austin Burt
    •  & Samantha O’Loughlin
  15. Department of Zoology, University of Oxford, The Tinbergen Building, South Parks Road, Oxford OX1 3PS, UK

    • H. Charles J. Godfray
  16. Department of Biology and School of Informatics and Computing, Indiana University, Bloomington, Indiana 47405, USA

    • Matthew W. Hahn
  17. KEMRI-Wellcome Trust Research Programme, PO Box 230, Bofa Road, Kilifi, Kenya

    • Janet Midega
    • , Charles Mbogo
    •  & Philip Bejon
  18. Global Health and Tropical Medicine, GHTM, Instituto de Higiene e Medicina Tropical, IHMT, Universidade Nova de Lisboa, UNL, Rua da Junqueira 100, 1349-008 Lisbon, Portugal

    • João Pinto
  19. Department of Microbiology and Immunology, Microbial and Plant Genomics Institute, University of Minnesota, St Paul, Minnesota 55108, USA

    • Michelle M. Riehle
  20. Unit for Genetics and Genomics of Insect Vectors, Institut Pasteur, Paris, France

    • Kenneth D. Vernick
  21. School of Natural Sciences and Psychology, Liverpool John Moores University, Liverpool L3 3AF, UK

    • Craig S. Wilding
  22. Department of Entomology, University of California, Riverside, California, USA

    • Bradley J. White
  23. Programa Nacional de Controle da Malária, Direcção Nacional de Saúde Pública, Ministério da Saúde, Luanda, Angola

    • Arlete D. Troco
  24. Institut de Recherche en Sciences de la Santé (IRSS), Bobo Dioulasso, Burkina Faso

    • Abdoulaye Diabaté
  25. Laboratoire de Recherche sur le Paludisme, Organisation de Coordination pour la lutte contre les Endémies en Afrique Centrale (OCEAC), Yaoundé, Cameroon

    • Carlo Costantini
  26. Malaria Research and Training Centre (MRTC), University of Bamako, Bamako, Mali

    • Boubacar Coulibaly
  27. Instituto Nacional de Saúde Pública, Ministério da Saúde Pública, Bissau, Guiné-Bissau

    • João Dinis
  28. Infectious Diseases Research Collaboration, 2C Nakasero Hill Road, PO Box 7475, Kampala, Uganda

    • Henry D. Mawejje
  29. The Broad Institute of Massachusetts Institute of Technology and Harvard, 415 Main Street, Cambridge, Massachusetts 02142, USA

    • Bronwyn MacInnis

Consortia

  1. The Anopheles gambiae 1000 Genomes Consortium

    Data analysis group

    Partner working group

    Sample collections—Angola:

    Burkina Faso:

    Cameroon:

    Gabon:

    Guinea:

    Guinea-Bissau:

    Kenya:

    Uganda:

    Crosses:

    Sequencing and data production

    Web application development

    Project coordination

Authors

    Contributions

    Details of author contributions are given in the consortium author list.

    Competing interests

    The author declare no competing financial interests.

    Corresponding authors

    Correspondence to Alistair Miles or Martin J. Donnelly or Mara K. N. Lawniczak or Dominic P. Kwiatkowski.

    Reviewer Information Nature thanks J. Pool and the other anonymous reviewer(s) for their contribution to the peer review of this work.

    Publisher's note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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      Supplementary Data

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      Supplementary Data

      This file contains Supplementary Table 3

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