Genetic diversity of the African malaria vector anopheles gambiae

Alistair Miles; Nicholas J. Harding; Giordano Bottà; Chris S. Clarkson; Tiago Antão; Krzysztof Kozak; Daniel R. Schrider; Andrew D. Kern; Seth Redmond; Igor Sharakhov; Richard D. Pearson; Christina Bergey; Michael C. Fontaine; Martin J. Donnelly; Mara K.N. Lawniczak; Diego Ayala; Nora J. Besansky; Austin Burt; Beniamino Caputo; Alessandra Della Torre; H. Charles J. Godfray; Matthew W. Hahn; Janet Midega; Daniel E. Neafsey; Samantha O'Loughlin; João Pinto; Michelle M. Riehle; Kenneth D. Vernick; David Weetman; Craig S. Wilding; Bradley J. White; Arlete D. Troco; Abdoulaye Diabaté; Carlo Costantini; Kyanne R. Rohatgi; Nohal Elissa; Boubacar Coulibaly; João Dinis; Charles Mbogo; Philip Bejon; Henry D. Mawejje; Jim Stalker; Kirk Rockett; Eleanor Drury; Daniel Mead; Anna Jeffreys; Christina Hubbart; Kate Rowlands; Alison T. Isaacs; Dushyanth Jyothi; Cinzia Malangone; Paul Vauterin; Ben Jeffery; Ian Wright; Lee Hart; Krzysztof Kluczyński; Victoria Cornelius; Bronwyn Macinnis; Christa Henrichs; Rachel Giacomantonio; Dominic P. Kwiatkowski

doi:10.1038/nature24995

Genetic diversity of the African malaria vector anopheles gambiae

Alistair Miles, Nicholas J. Harding, Giordano Bottà, Chris S. Clarkson, Tiago Antão, Krzysztof Kozak, Daniel R. Schrider, Andrew D. Kern, Seth Redmond, Igor Sharakhov, Richard D. Pearson, Christina Bergey, Michael C. Fontaine, Martin J. Donnelly, Mara K.N. Lawniczak, Diego Ayala, Nora J. Besansky, Austin Burt, Beniamino Caputo, Alessandra Della TorreH. Charles J. Godfray, Matthew W. Hahn, Janet Midega, Daniel E. Neafsey, Samantha O'Loughlin, João Pinto, Michelle M. Riehle, Kenneth D. Vernick, David Weetman, Craig S. Wilding, Bradley J. White, Arlete D. Troco, Abdoulaye Diabaté, Carlo Costantini, Kyanne R. Rohatgi, Nohal Elissa, Boubacar Coulibaly, João Dinis, Charles Mbogo, Philip Bejon, Henry D. Mawejje, Jim Stalker, Kirk Rockett, Eleanor Drury, Daniel Mead, Anna Jeffreys, Christina Hubbart, Kate Rowlands, Alison T. Isaacs, Dushyanth Jyothi, Cinzia Malangone, Paul Vauterin, Ben Jeffery, Ian Wright, Lee Hart, Krzysztof Kluczyński, Victoria Cornelius, Bronwyn Macinnis, Christa Henrichs, Rachel Giacomantonio, Dominic P. Kwiatkowski

Microbiology

Research output: Contribution to journal › Article › peer-review

97 Scopus citations

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.

Original language	English (US)
Pages (from-to)	96-100
Number of pages	5
Journal	Nature
Volume	552
DOIs	https://doi.org/10.1038/nature24995
State	Published - Dec 7 2017

Bibliographical note

Funding Information:
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.

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Miles, A., Harding, N. J., Bottà, G., Clarkson, C. S., Antão, T., Kozak, K., Schrider, D. R., Kern, A. D., Redmond, S., Sharakhov, I., Pearson, R. D., Bergey, C., Fontaine, M. C., Donnelly, M. J., Lawniczak, M. K. N., Ayala, D., Besansky, N. J., Burt, A., Caputo, B., ... Kwiatkowski, D. P. (2017). Genetic diversity of the African malaria vector anopheles gambiae. Nature, 552, 96-100. https://doi.org/10.1038/nature24995

Genetic diversity of the African malaria vector anopheles gambiae. / Miles, Alistair; Harding, Nicholas J.; Bottà, Giordano; Clarkson, Chris S.; Antão, Tiago; Kozak, Krzysztof; Schrider, Daniel R.; Kern, Andrew D.; Redmond, Seth; Sharakhov, Igor; Pearson, Richard D.; Bergey, Christina; Fontaine, Michael C.; Donnelly, Martin J.; Lawniczak, Mara K.N.; Ayala, Diego; Besansky, Nora J.; Burt, Austin; Caputo, Beniamino; Torre, Alessandra Della; Godfray, H. Charles J.; Hahn, Matthew W.; Midega, Janet; Neafsey, Daniel E.; O'Loughlin, Samantha; Pinto, João; Riehle, Michelle M.; Vernick, Kenneth D.; Weetman, David; Wilding, Craig S.; White, Bradley J.; Troco, Arlete D.; Diabaté, Abdoulaye; Costantini, Carlo; Rohatgi, Kyanne R.; Elissa, Nohal; Coulibaly, Boubacar; Dinis, João; Mbogo, Charles; Bejon, Philip; Mawejje, Henry D.; Stalker, Jim; Rockett, Kirk; Drury, Eleanor; Mead, Daniel; Jeffreys, Anna; Hubbart, Christina; Rowlands, Kate; Isaacs, Alison T.; Jyothi, Dushyanth; Malangone, Cinzia; Vauterin, Paul; Jeffery, Ben; Wright, Ian; Hart, Lee; Kluczyński, Krzysztof; Cornelius, Victoria; Macinnis, Bronwyn; Henrichs, Christa; Giacomantonio, Rachel; Kwiatkowski, Dominic P.

In: Nature, Vol. 552, 07.12.2017, p. 96-100.

Research output: Contribution to journal › Article › peer-review

Miles, A, Harding, NJ, Bottà, G, Clarkson, CS, Antão, T, Kozak, K, Schrider, DR, Kern, AD, Redmond, S, Sharakhov, I, Pearson, RD, Bergey, C, Fontaine, MC, Donnelly, MJ, Lawniczak, MKN, Ayala, D, Besansky, NJ, Burt, A, Caputo, B, Torre, AD, Godfray, HCJ, Hahn, MW, Midega, J, Neafsey, DE, O'Loughlin, S, Pinto, J, Riehle, MM, Vernick, KD, Weetman, D, Wilding, CS, White, BJ, Troco, AD, Diabaté, A, Costantini, C, Rohatgi, KR, Elissa, N, Coulibaly, B, Dinis, J, Mbogo, C, Bejon, P, Mawejje, HD, Stalker, J, Rockett, K, Drury, E, Mead, D, Jeffreys, A, Hubbart, C, Rowlands, K, Isaacs, AT, Jyothi, D, Malangone, C, Vauterin, P, Jeffery, B, Wright, I, Hart, L, Kluczyński, K, Cornelius, V, Macinnis, B, Henrichs, C, Giacomantonio, R & Kwiatkowski, DP 2017, 'Genetic diversity of the African malaria vector anopheles gambiae', Nature, vol. 552, pp. 96-100. https://doi.org/10.1038/nature24995

Miles, Alistair ; Harding, Nicholas J. ; Bottà, Giordano ; Clarkson, Chris S. ; Antão, Tiago ; Kozak, Krzysztof ; Schrider, Daniel R. ; Kern, Andrew D. ; Redmond, Seth ; Sharakhov, Igor ; Pearson, Richard D. ; Bergey, Christina ; Fontaine, Michael C. ; Donnelly, Martin J. ; Lawniczak, Mara K.N. ; Ayala, Diego ; Besansky, Nora J. ; Burt, Austin ; Caputo, Beniamino ; Torre, Alessandra Della ; Godfray, H. Charles J. ; Hahn, Matthew W. ; Midega, Janet ; Neafsey, Daniel E. ; O'Loughlin, Samantha ; Pinto, João ; Riehle, Michelle M. ; Vernick, Kenneth D. ; Weetman, David ; Wilding, Craig S. ; White, Bradley J. ; Troco, Arlete D. ; Diabaté, Abdoulaye ; Costantini, Carlo ; Rohatgi, Kyanne R. ; Elissa, Nohal ; Coulibaly, Boubacar ; Dinis, João ; Mbogo, Charles ; Bejon, Philip ; Mawejje, Henry D. ; Stalker, Jim ; Rockett, Kirk ; Drury, Eleanor ; Mead, Daniel ; Jeffreys, Anna ; Hubbart, Christina ; Rowlands, Kate ; Isaacs, Alison T. ; Jyothi, Dushyanth ; Malangone, Cinzia ; Vauterin, Paul ; Jeffery, Ben ; Wright, Ian ; Hart, Lee ; Kluczyński, Krzysztof ; Cornelius, Victoria ; Macinnis, Bronwyn ; Henrichs, Christa ; Giacomantonio, Rachel ; Kwiatkowski, Dominic P. / Genetic diversity of the African malaria vector anopheles gambiae. In: Nature. 2017 ; Vol. 552. pp. 96-100.

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title = "Genetic diversity of the African malaria vector anopheles gambiae",

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.",

author = "Alistair Miles and Harding, {Nicholas J.} and Giordano Bott{\`a} and Clarkson, {Chris S.} and Tiago Ant{\~a}o and Krzysztof Kozak and Schrider, {Daniel R.} and Kern, {Andrew D.} and Seth Redmond and Igor Sharakhov and Pearson, {Richard D.} and Christina Bergey and Fontaine, {Michael C.} and Donnelly, {Martin J.} and Lawniczak, {Mara K.N.} and Diego Ayala and Besansky, {Nora J.} and Austin Burt and Beniamino Caputo and Torre, {Alessandra Della} and Godfray, {H. Charles J.} and Hahn, {Matthew W.} and Janet Midega and Neafsey, {Daniel E.} and Samantha O'Loughlin and Jo{\~a}o Pinto and Riehle, {Michelle M.} and Vernick, {Kenneth D.} and David Weetman and Wilding, {Craig S.} and White, {Bradley J.} and Troco, {Arlete D.} and Abdoulaye Diabat{\'e} and Carlo Costantini and Rohatgi, {Kyanne R.} and Nohal Elissa and Boubacar Coulibaly and Jo{\~a}o Dinis and Charles Mbogo and Philip Bejon and Mawejje, {Henry D.} and Jim Stalker and Kirk Rockett and Eleanor Drury and Daniel Mead and Anna Jeffreys and Christina Hubbart and Kate Rowlands and Isaacs, {Alison T.} and Dushyanth Jyothi and Cinzia Malangone and Paul Vauterin and Ben Jeffery and Ian Wright and Lee Hart and Krzysztof Kluczy{\'n}ski and Victoria Cornelius and Bronwyn Macinnis and Christa Henrichs and Rachel Giacomantonio and Kwiatkowski, {Dominic P.}",

note = "Funding Information: 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.{\textquoteright}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.",

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T1 - Genetic diversity of the African malaria vector anopheles gambiae

AU - Miles, Alistair

AU - Harding, Nicholas J.

AU - Bottà, Giordano

AU - Clarkson, Chris S.

AU - Antão, Tiago

AU - Kozak, Krzysztof

AU - Schrider, Daniel R.

AU - Kern, Andrew D.

AU - Redmond, Seth

AU - Sharakhov, Igor

AU - Pearson, Richard D.

AU - Bergey, Christina

AU - Fontaine, Michael C.

AU - Donnelly, Martin J.

AU - Lawniczak, Mara K.N.

AU - Ayala, Diego

AU - Besansky, Nora J.

AU - Burt, Austin

AU - Caputo, Beniamino

AU - Torre, Alessandra Della

AU - Godfray, H. Charles J.

AU - Hahn, Matthew W.

AU - Midega, Janet

AU - Neafsey, Daniel E.

AU - O'Loughlin, Samantha

AU - Pinto, João

AU - Riehle, Michelle M.

AU - Vernick, Kenneth D.

AU - Weetman, David

AU - Wilding, Craig S.

AU - White, Bradley J.

AU - Troco, Arlete D.

AU - Diabaté, Abdoulaye

AU - Costantini, Carlo

AU - Rohatgi, Kyanne R.

AU - Elissa, Nohal

AU - Coulibaly, Boubacar

AU - Dinis, João

AU - Mbogo, Charles

AU - Bejon, Philip

AU - Mawejje, Henry D.

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AU - Drury, Eleanor

AU - Mead, Daniel

AU - Jeffreys, Anna

AU - Hubbart, Christina

AU - Rowlands, Kate

AU - Isaacs, Alison T.

AU - Jyothi, Dushyanth

AU - Malangone, Cinzia

AU - Vauterin, Paul

AU - Jeffery, Ben

AU - Wright, Ian

AU - Hart, Lee

AU - Kluczyński, Krzysztof

AU - Cornelius, Victoria

AU - Macinnis, Bronwyn

AU - Henrichs, Christa

AU - Giacomantonio, Rachel

AU - Kwiatkowski, Dominic P.

N1 - Funding Information: 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.

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N2 - 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.

AB - 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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