Highly evolvable malaria vectors: The genomes of 16 Anopheles mosquitoes

Daniel E. Neafsey; Robert M. Waterhouse; Mohammad R. Abai; Sergey S. Aganezov; Max A. Alekseyev; James E. Allen; James Amon; Bruno Arcà; Peter Arensburger; Gleb Artemov; Lauren A. Assour; Hamidreza Basseri; Aaron Berlin; Bruce W. Birren; Stephanie A. Blandin; Andrew I. Brockman; Thomas R. Burkot; Austin Burt; Clara S. Chan; Cedric Chauve; Joanna C. Chiu; Mikkel Christensen; Carlo Costantini; Victoria L.M. Davidson; Elena Deligianni; Tania Dottorini; Vicky Dritsou; Stacey B. Gabriel; Wamdaogo M. Guelbeogo; Andrew B. Hall; Mira V. Han; Thaung Hlaing; Daniel S.T. Hughes; Adam M. Jenkins; Xiaofang Jiang; Irwin Jungreis; Evdoxia G. Kakani; Maryam Kamali; Petri Kemppainen; Ryan C. Kennedy; Ioannis K. Kirmitzoglou; Lizette L. Koekemoer; Njoroge Laban; Nicholas Langridge; Mara K.N. Lawniczak; Manolis Lirakis; Neil F. Lobo; Ernesto Lowy; Robert M. MacCallum; Chunhong Mao; Gareth Maslen; Charles Mbogo; Jenny McCarthy; Kristin Michel; Sara N. Mitchell; Wendy Moore; Katherine A. Murphy; Anastasia N. Naumenko; Tony Nolan; Eva M. Novoa; Samantha O'Loughlin; Chioma Oringanje; Mohammad A. Oshaghi; Nazzy Pakpour; Philippos A. Papathanos; Ashley N. Peery; Michael Povelones; Anil Prakash; David P. Price; Ashok Rajaraman; Lisa Reimer; David C. Rinker; Antonis Rokas; Tanya L. Russell; N'Fale Sagnon; Maria V. Sharakhova; Terrance Shea; Felipe A. Simão; Frederic Simard; Michel A. Slotman; Pradya Somboon; Vladimir Stegniy; Claudio J. Struchiner; Gregg W.C. Thomas; Marta Tojo; Pantelis Topalis; José M.C. Tubio; Maria F. Unger; John Vontas; Catherine Walton; Craig S. Wilding; Judith H. Willis; Yi Chieh Wu; Guiyun Yan; Evgeny M. Zdobnov; Xiaofan Zhou; Flaminia Catteruccia; George K. Christophides; Frank H. Collins; Robert S. Cornman; Andrea Crisanti; Martin Donnelly; Scott J. Emrich; Michael C. Fontaine; William Gelbart; Matthew W. Hahn; Immo A. Hansen; Paul I. Howell; Fotis C. Kafatos; Manolis Kellis; Daniel Lawson; Christos Louis; Shirley Luckhart; Marc A.T. Muskavitch; José M. Ribeiro; Michael A. Riehle; Igor V. Sharakhov; Zhijian Tu; Laurence J. Zwiebel; Nora J. Besansky

doi:10.1126/science.1258522

Highly evolvable malaria vectors: The genomes of 16 Anopheles mosquitoes

Daniel E. Neafsey
, Robert M. Waterhouse
, Mohammad R. Abai
, Sergey S. Aganezov
, Max A. Alekseyev
, James E. Allen
, James Amon
, Bruno Arcà
, Peter Arensburger
, Gleb Artemov
, Lauren A. Assour
, Hamidreza Basseri
, Aaron Berlin
, Bruce W. Birren
, Stephanie A. Blandin
, Andrew I. Brockman
, Thomas R. Burkot
, Austin Burt
, Clara S. Chan
, Cedric Chauve

Joanna C. Chiu, Mikkel Christensen, Carlo Costantini, Victoria L.M. Davidson, Elena Deligianni, Tania Dottorini, Vicky Dritsou, Stacey B. Gabriel, Wamdaogo M. Guelbeogo, Andrew B. Hall, Mira V. Han, Thaung Hlaing, Daniel S.T. Hughes, Adam M. Jenkins, Xiaofang Jiang, Irwin Jungreis, Evdoxia G. Kakani, Maryam Kamali, Petri Kemppainen, Ryan C. Kennedy, Ioannis K. Kirmitzoglou, Lizette L. Koekemoer, Njoroge Laban, Nicholas Langridge, Mara K.N. Lawniczak, Manolis Lirakis, Neil F. Lobo, Ernesto Lowy, Robert M. MacCallum, Chunhong Mao, Gareth Maslen, Charles Mbogo, Jenny McCarthy, Kristin Michel, Sara N. Mitchell, Wendy Moore, Katherine A. Murphy, Anastasia N. Naumenko, Tony Nolan, Eva M. Novoa, Samantha O'Loughlin, Chioma Oringanje, Mohammad A. Oshaghi, Nazzy Pakpour, Philippos A. Papathanos, Ashley N. Peery, Michael Povelones, Anil Prakash, David P. Price, Ashok Rajaraman, Lisa Reimer, David C. Rinker, Antonis Rokas, Tanya L. Russell, N'Fale Sagnon, Maria V. Sharakhova, Terrance Shea, Felipe A. Simão, Frederic Simard, Michel A. Slotman, Pradya Somboon, Vladimir Stegniy, Claudio J. Struchiner, Gregg W.C. Thomas, Marta Tojo, Pantelis Topalis, José M.C. Tubio, Maria F. Unger, John Vontas, Catherine Walton, Craig S. Wilding, Judith H. Willis, Yi Chieh Wu, Guiyun Yan, Evgeny M. Zdobnov, Xiaofan Zhou, Flaminia Catteruccia, George K. Christophides, Frank H. Collins, Robert S. Cornman, Andrea Crisanti, Martin Donnelly, Scott J. Emrich, Michael C. Fontaine, William Gelbart, Matthew W. Hahn, Immo A. Hansen, Paul I. Howell, Fotis C. Kafatos, Manolis Kellis, Daniel Lawson, Christos Louis, Shirley Luckhart, Marc A.T. Muskavitch, José M. Ribeiro, Michael A. Riehle, Igor V. Sharakhov, Zhijian Tu, Laurence J. Zwiebel, Nora J. Besansky

Vector Biology

Broad Institute
Massachusetts Institute of Technology
University of Geneva
Swiss Institute of Bioinformatics
Tehran University of Medical Sciences
George Washington University
European Molecular Biology Laboratory
Ministry of Health
University of Rome La Sapienza
California State Polytechnic University Pomona
Tomsk State University
University of Notre Dame
Institut national de la santé et de la recherche médicale
Centre national de la Recherche Scientifique
Imperial College London
James Cook University Queensland
Simon Fraser University
University of California at Davis
Institut de recherche pour le développement
Kansas State University
Foundation for Research and Technology-Hellas
University of Perugia
Centre national de recherche et de formation sur le paludisme
Virginia Polytechnic Institute and State University
University of Nevada, Las Vegas
Department of Medical Research
Baylor College of Medicine
Boston College
Harvard University
University of Manchester
University of California at San Francisco
University of Cyprus
National Health Laboratory Services
National Museums of Kenya
University of Crete
Wellcome Trust Research Laboratories Nairobi
University of Arizona
University of Pennsylvania
Indian Council of Medical Research
New Mexico State University
Vanderbilt University
Texas A&M University
Chiang Mai University
Fundação Oswaldo Cruz
Universidade do Estado do Rio de Janeiro
Indiana University Bloomington
University of Santiago de Compostela
Wellcome Sanger Institute
Liverpool John Moores University
University of Georgia
Harvey Mudd College
University of California at Irvine
University of Groningen
Centers for Disease Control and Prevention
Biogen IDEC
National Institutes of Health

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

453 Citations (Scopus)

Abstract

Variation in vectorial capacity for human malaria among Anopheles mosquito species is determined by many factors, including behavior, immunity, and life history. To investigate the genomic basis of vectorial capacity and explore new avenues for vector control, we sequenced the genomes of 16 anopheline mosquito species from diverse locations spanning ~100 million years of evolution. Comparative analyses show faster rates of gene gain and loss, elevated gene shuffling on the X chromosome, and more intron losses, relative to Drosophila. Some determinants of vectorial capacity, such as chemosensory genes, do not show elevated turnover but instead diversify through protein-sequence changes. This dynamism of anopheline genes and genomes may contribute to their flexible capacity to take advantage of new ecological niches, including adapting to humans as primary hosts.

Original language	English
Article number	1258522
Pages (from-to)	1258522
Journal	Science
Volume	347
Issue number	6217
DOIs	https://doi.org/10.1126/science.1258522
Publication status	Published - 27 Nov 2014

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

SDG 3 Good Health and Well-being

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10.1126/science.1258522

Cite this

Neafsey, D. E., Waterhouse, R. M., Abai, M. R., Aganezov, S. S., Alekseyev, M. A., Allen, J. E., Amon, J., Arcà, B., Arensburger, P., Artemov, G., Assour, L. A., Basseri, H., Berlin, A., Birren, B. W., Blandin, S. A., Brockman, A. I., Burkot, T. R., Burt, A., Chan, C. S., ... Besansky, N. J. (2014). Highly evolvable malaria vectors: The genomes of 16 Anopheles mosquitoes. Science, 347(6217), 1258522. Article 1258522. https://doi.org/10.1126/science.1258522

@article{ef323a7d444b429c997e6ad31fba947b,

title = "Highly evolvable malaria vectors: The genomes of 16 Anopheles mosquitoes",

abstract = "Variation in vectorial capacity for human malaria among Anopheles mosquito species is determined by many factors, including behavior, immunity, and life history. To investigate the genomic basis of vectorial capacity and explore new avenues for vector control, we sequenced the genomes of 16 anopheline mosquito species from diverse locations spanning \textasciitilde{}100 million years of evolution. Comparative analyses show faster rates of gene gain and loss, elevated gene shuffling on the X chromosome, and more intron losses, relative to Drosophila. Some determinants of vectorial capacity, such as chemosensory genes, do not show elevated turnover but instead diversify through protein-sequence changes. This dynamism of anopheline genes and genomes may contribute to their flexible capacity to take advantage of new ecological niches, including adapting to humans as primary hosts.",

author = "Neafsey, \{Daniel E.\} and Waterhouse, \{Robert M.\} and Abai, \{Mohammad R.\} and Aganezov, \{Sergey S.\} and Alekseyev, \{Max A.\} and Allen, \{James E.\} and James Amon and Bruno Arc{\`a} and Peter Arensburger and Gleb Artemov and Assour, \{Lauren A.\} and Hamidreza Basseri and Aaron Berlin and Birren, \{Bruce W.\} and Blandin, \{Stephanie A.\} and Brockman, \{Andrew I.\} and Burkot, \{Thomas R.\} and Austin Burt and Chan, \{Clara S.\} and Cedric Chauve and Chiu, \{Joanna C.\} and Mikkel Christensen and Carlo Costantini and Davidson, \{Victoria L.M.\} and Elena Deligianni and Tania Dottorini and Vicky Dritsou and Gabriel, \{Stacey B.\} and Guelbeogo, \{Wamdaogo M.\} and Hall, \{Andrew B.\} and Han, \{Mira V.\} and Thaung Hlaing and Hughes, \{Daniel S.T.\} and Jenkins, \{Adam M.\} and Xiaofang Jiang and Irwin Jungreis and Kakani, \{Evdoxia G.\} and Maryam Kamali and Petri Kemppainen and Kennedy, \{Ryan C.\} and Kirmitzoglou, \{Ioannis K.\} and Koekemoer, \{Lizette L.\} and Njoroge Laban and Nicholas Langridge and Lawniczak, \{Mara K.N.\} and Manolis Lirakis and Lobo, \{Neil F.\} and Ernesto Lowy and MacCallum, \{Robert M.\} and Chunhong Mao and Gareth Maslen and Charles Mbogo and Jenny McCarthy and Kristin Michel and Mitchell, \{Sara N.\} and Wendy Moore and Murphy, \{Katherine A.\} and Naumenko, \{Anastasia N.\} and Tony Nolan and Novoa, \{Eva M.\} and Samantha O'Loughlin and Chioma Oringanje and Oshaghi, \{Mohammad A.\} and Nazzy Pakpour and Papathanos, \{Philippos A.\} and Peery, \{Ashley N.\} and Michael Povelones and Anil Prakash and Price, \{David P.\} and Ashok Rajaraman and Lisa Reimer and Rinker, \{David C.\} and Antonis Rokas and Russell, \{Tanya L.\} and N'Fale Sagnon and Sharakhova, \{Maria V.\} and Terrance Shea and Sim{\~a}o, \{Felipe A.\} and Frederic Simard and Slotman, \{Michel A.\} and Pradya Somboon and Vladimir Stegniy and Struchiner, \{Claudio J.\} and Thomas, \{Gregg W.C.\} and Marta Tojo and Pantelis Topalis and Tubio, \{Jos{\'e} M.C.\} and Unger, \{Maria F.\} and John Vontas and Catherine Walton and Wilding, \{Craig S.\} and Willis, \{Judith H.\} and Wu, \{Yi Chieh\} and Guiyun Yan and Zdobnov, \{Evgeny M.\} and Xiaofan Zhou and Flaminia Catteruccia and Christophides, \{George K.\} and Collins, \{Frank H.\} and Cornman, \{Robert S.\} and Andrea Crisanti and Martin Donnelly and Emrich, \{Scott J.\} and Fontaine, \{Michael C.\} and William Gelbart and Hahn, \{Matthew W.\} and Hansen, \{Immo A.\} and Howell, \{Paul I.\} and Kafatos, \{Fotis C.\} and Manolis Kellis and Daniel Lawson and Christos Louis and Shirley Luckhart and Muskavitch, \{Marc A.T.\} and Ribeiro, \{Jos{\'e} M.\} and Riehle, \{Michael A.\} and Sharakhov, \{Igor V.\} and Zhijian Tu and Zwiebel, \{Laurence J.\} and Besansky, \{Nora J.\}",

year = "2014",

month = nov,

day = "27",

doi = "10.1126/science.1258522",

language = "English",

volume = "347",

pages = "1258522",

journal = "Science",

issn = "0036-8075",

publisher = "American Association for the Advancement of Science",

number = "6217",

}

Neafsey, DE, Waterhouse, RM, Abai, MR, Aganezov, SS, Alekseyev, MA, Allen, JE, Amon, J, Arcà, B, Arensburger, P, Artemov, G, Assour, LA, Basseri, H, Berlin, A, Birren, BW, Blandin, SA, Brockman, AI, Burkot, TR, Burt, A, Chan, CS, Chauve, C, Chiu, JC, Christensen, M, Costantini, C, Davidson, VLM, Deligianni, E, Dottorini, T, Dritsou, V, Gabriel, SB, Guelbeogo, WM, Hall, AB, Han, MV, Hlaing, T, Hughes, DST, Jenkins, AM, Jiang, X, Jungreis, I, Kakani, EG, Kamali, M, Kemppainen, P, Kennedy, RC, Kirmitzoglou, IK, Koekemoer, LL, Laban, N, Langridge, N, Lawniczak, MKN, Lirakis, M, Lobo, NF, Lowy, E, MacCallum, RM, Mao, C, Maslen, G, Mbogo, C, McCarthy, J, Michel, K, Mitchell, SN, Moore, W, Murphy, KA, Naumenko, AN, Nolan, T, Novoa, EM, O'Loughlin, S, Oringanje, C, Oshaghi, MA, Pakpour, N, Papathanos, PA, Peery, AN, Povelones, M, Prakash, A, Price, DP, Rajaraman, A, Reimer, L, Rinker, DC, Rokas, A, Russell, TL, Sagnon, NF, Sharakhova, MV, Shea, T, Simão, FA, Simard, F, Slotman, MA, Somboon, P, Stegniy, V, Struchiner, CJ, Thomas, GWC, Tojo, M, Topalis, P, Tubio, JMC, Unger, MF, Vontas, J, Walton, C, Wilding, CS, Willis, JH, Wu, YC, Yan, G, Zdobnov, EM, Zhou, X, Catteruccia, F, Christophides, GK, Collins, FH, Cornman, RS, Crisanti, A, Donnelly, M, Emrich, SJ, Fontaine, MC, Gelbart, W, Hahn, MW, Hansen, IA, Howell, PI, Kafatos, FC, Kellis, M, Lawson, D, Louis, C, Luckhart, S, Muskavitch, MAT, Ribeiro, JM, Riehle, MA, Sharakhov, IV, Tu, Z, Zwiebel, LJ & Besansky, NJ 2014, 'Highly evolvable malaria vectors: The genomes of 16 Anopheles mosquitoes', Science, vol. 347, no. 6217, 1258522, pp. 1258522. https://doi.org/10.1126/science.1258522

TY - JOUR

T1 - Highly evolvable malaria vectors: The genomes of 16 Anopheles mosquitoes

AU - Neafsey, Daniel E.

AU - Waterhouse, Robert M.

AU - Abai, Mohammad R.

AU - Aganezov, Sergey S.

AU - Alekseyev, Max A.

AU - Allen, James E.

AU - Amon, James

AU - Arcà, Bruno

AU - Arensburger, Peter

AU - Artemov, Gleb

AU - Assour, Lauren A.

AU - Basseri, Hamidreza

AU - Berlin, Aaron

AU - Birren, Bruce W.

AU - Blandin, Stephanie A.

AU - Brockman, Andrew I.

AU - Burkot, Thomas R.

AU - Burt, Austin

AU - Chan, Clara S.

AU - Chauve, Cedric

AU - Chiu, Joanna C.

AU - Christensen, Mikkel

AU - Costantini, Carlo

AU - Davidson, Victoria L.M.

AU - Deligianni, Elena

AU - Dottorini, Tania

AU - Dritsou, Vicky

AU - Gabriel, Stacey B.

AU - Guelbeogo, Wamdaogo M.

AU - Hall, Andrew B.

AU - Han, Mira V.

AU - Hlaing, Thaung

AU - Hughes, Daniel S.T.

AU - Jenkins, Adam M.

AU - Jiang, Xiaofang

AU - Jungreis, Irwin

AU - Kakani, Evdoxia G.

AU - Kamali, Maryam

AU - Kemppainen, Petri

AU - Kennedy, Ryan C.

AU - Kirmitzoglou, Ioannis K.

AU - Koekemoer, Lizette L.

AU - Laban, Njoroge

AU - Langridge, Nicholas

AU - Lawniczak, Mara K.N.

AU - Lirakis, Manolis

AU - Lobo, Neil F.

AU - Lowy, Ernesto

AU - MacCallum, Robert M.

AU - Mao, Chunhong

AU - Maslen, Gareth

AU - Mbogo, Charles

AU - McCarthy, Jenny

AU - Michel, Kristin

AU - Mitchell, Sara N.

AU - Moore, Wendy

AU - Murphy, Katherine A.

AU - Naumenko, Anastasia N.

AU - Nolan, Tony

AU - Novoa, Eva M.

AU - O'Loughlin, Samantha

AU - Oringanje, Chioma

AU - Oshaghi, Mohammad A.

AU - Pakpour, Nazzy

AU - Papathanos, Philippos A.

AU - Peery, Ashley N.

AU - Povelones, Michael

AU - Prakash, Anil

AU - Price, David P.

AU - Rajaraman, Ashok

AU - Reimer, Lisa

AU - Rinker, David C.

AU - Rokas, Antonis

AU - Russell, Tanya L.

AU - Sagnon, N'Fale

AU - Sharakhova, Maria V.

AU - Shea, Terrance

AU - Simão, Felipe A.

AU - Simard, Frederic

AU - Slotman, Michel A.

AU - Somboon, Pradya

AU - Stegniy, Vladimir

AU - Struchiner, Claudio J.

AU - Thomas, Gregg W.C.

AU - Tojo, Marta

AU - Topalis, Pantelis

AU - Tubio, José M.C.

AU - Unger, Maria F.

AU - Vontas, John

AU - Walton, Catherine

AU - Wilding, Craig S.

AU - Willis, Judith H.

AU - Wu, Yi Chieh

AU - Yan, Guiyun

AU - Zdobnov, Evgeny M.

AU - Zhou, Xiaofan

AU - Catteruccia, Flaminia

AU - Christophides, George K.

AU - Collins, Frank H.

AU - Cornman, Robert S.

AU - Crisanti, Andrea

AU - Donnelly, Martin

AU - Emrich, Scott J.

AU - Fontaine, Michael C.

AU - Gelbart, William

AU - Hahn, Matthew W.

AU - Hansen, Immo A.

AU - Howell, Paul I.

AU - Kafatos, Fotis C.

AU - Kellis, Manolis

AU - Lawson, Daniel

AU - Louis, Christos

AU - Luckhart, Shirley

AU - Muskavitch, Marc A.T.

AU - Ribeiro, José M.

AU - Riehle, Michael A.

AU - Sharakhov, Igor V.

AU - Tu, Zhijian

AU - Zwiebel, Laurence J.

AU - Besansky, Nora J.

PY - 2014/11/27

Y1 - 2014/11/27

N2 - Variation in vectorial capacity for human malaria among Anopheles mosquito species is determined by many factors, including behavior, immunity, and life history. To investigate the genomic basis of vectorial capacity and explore new avenues for vector control, we sequenced the genomes of 16 anopheline mosquito species from diverse locations spanning ~100 million years of evolution. Comparative analyses show faster rates of gene gain and loss, elevated gene shuffling on the X chromosome, and more intron losses, relative to Drosophila. Some determinants of vectorial capacity, such as chemosensory genes, do not show elevated turnover but instead diversify through protein-sequence changes. This dynamism of anopheline genes and genomes may contribute to their flexible capacity to take advantage of new ecological niches, including adapting to humans as primary hosts.

AB - Variation in vectorial capacity for human malaria among Anopheles mosquito species is determined by many factors, including behavior, immunity, and life history. To investigate the genomic basis of vectorial capacity and explore new avenues for vector control, we sequenced the genomes of 16 anopheline mosquito species from diverse locations spanning ~100 million years of evolution. Comparative analyses show faster rates of gene gain and loss, elevated gene shuffling on the X chromosome, and more intron losses, relative to Drosophila. Some determinants of vectorial capacity, such as chemosensory genes, do not show elevated turnover but instead diversify through protein-sequence changes. This dynamism of anopheline genes and genomes may contribute to their flexible capacity to take advantage of new ecological niches, including adapting to humans as primary hosts.

U2 - 10.1126/science.1258522

DO - 10.1126/science.1258522

M3 - Article

SN - 0036-8075

VL - 347

SP - 1258522

JO - Science

JF - Science

IS - 6217

M1 - 1258522

ER -

Highly evolvable malaria vectors: The genomes of 16 Anopheles mosquitoes

Abstract

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