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 ChauveJoanna 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 J. 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 J. 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

Research output: Contribution to journalArticle

220 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 languageEnglish (US)
Article number1258522
JournalScience
Volume347
Issue number6217
DOIs
StatePublished - Jan 2 2015

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Anopheles
Culicidae
Malaria
Genome
Genes
X Chromosome
Introns
Drosophila
Immunity
Proteins

ASJC Scopus subject areas

  • General
  • Medicine(all)

Cite this

Neafsey, D. E., Waterhouse, R. M., Abai, M. R., Aganezov, S. S., Alekseyev, M. A., Allen, J. E., ... Besansky, N. J. (2015). Highly evolvable malaria vectors: The genomes of 16 Anopheles mosquitoes. Science, 347(6217), [1258522]. https://doi.org/10.1126/science.1258522

Highly evolvable malaria vectors : The genomes of 16 Anopheles mosquitoes. / Neafsey, Daniel E.; Waterhouse, Robert M.; Abai, Mohammad R.; Aganezov, Sergey S.; Alekseyev, Max A.; Allen, James E.; Amon, James; Arcà, Bruno; Arensburger, Peter; Artemov, Gleb; Assour, Lauren A.; Basseri, Hamidreza; Berlin, Aaron; Birren, Bruce W.; Blandin, Stephanie A.; Brockman, Andrew I.; Burkot, Thomas R.; Burt, Austin; Chan, Clara S.; Chauve, Cedric; Chiu, Joanna C.; Christensen, Mikkel; Costantini, Carlo; Davidson, Victoria L M; Deligianni, Elena; Dottorini, Tania; Dritsou, Vicky; Gabriel, Stacey B.; Guelbeogo, Wamdaogo M.; Hall, Andrew B.; Han, Mira V.; Hlaing, Thaung; Hughes, Daniel S T; Jenkins, Adam M.; Jiang, Xiaofang; Jungreis, Irwin; Kakani, Evdoxia G.; Kamali, Maryam; Kemppainen, Petri; Kennedy, Ryan C.; Kirmitzoglou, Ioannis K.; Koekemoer, Lizette L.; Laban, Njoroge; Langridge, Nicholas; Lawniczak, Mara K N; Lirakis, Manolis; Lobo, Neil F.; Lowy, Ernesto; MacCallum, Robert M.; Mao, Chunhong; Maslen, Gareth; Mbogo, Charles; McCarthy, Jenny; Michel, Kristin; Mitchell, Sara N.; Moore, Wendy; Murphy, Katherine A.; Naumenko, Anastasia N.; Nolan, Tony; Novoa, Eva M.; O'Loughlin, Samantha; Oringanje, Chioma; Oshaghi, Mohammad A.; Pakpour, Nazzy; Papathanos, Philippos A.; Peery, Ashley N.; Povelones, Michael; Prakash, Anil; Price, David P.; Rajaraman, Ashok; Reimer, Lisa J.; Rinker, David C.; Rokas, Antonis; Russell, Tanya L.; Sagnon, N'Fale; Sharakhova, Maria V.; Shea, Terrance; Simão, Felipe A.; Simard, Frederic; Slotman, Michel A.; Somboon, Pradya; Stegniy, Vladimir; Struchiner, Claudio J.; Thomas, Gregg W C; Tojo, Marta; Topalis, Pantelis; Tubio, José M C; Unger, Maria F.; Vontas, John; Walton, Catherine; Wilding, Craig S.; Willis, Judith H.; Wu, Yi Chieh; Yan, Guiyun; Zdobnov, Evgeny M.; Zhou, Xiaofan; Catteruccia, Flaminia; Christophides, George K.; Collins, Frank H.; Cornman, Robert S.; Crisanti, Andrea; Donnelly, Martin J.; Emrich, Scott J.; Fontaine, Michael C.; Gelbart, William; Hahn, Matthew W.; Hansen, Immo A.; Howell, Paul I.; Kafatos, Fotis C.; Kellis, Manolis; Lawson, Daniel; Louis, Christos; Luckhart, Shirley; Muskavitch, Marc A T; Ribeiro, José M.; Riehle, Michael A.; Sharakhov, Igor V.; Tu, Zhijian; Zwiebel, Laurence J.; Besansky, Nora J.

In: Science, Vol. 347, No. 6217, 1258522, 02.01.2015.

Research output: Contribution to journalArticle

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, LJ, 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, MJ, 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 2015, 'Highly evolvable malaria vectors: The genomes of 16 Anopheles mosquitoes', Science, vol. 347, no. 6217, 1258522. https://doi.org/10.1126/science.1258522
Neafsey DE, Waterhouse RM, Abai MR, Aganezov SS, Alekseyev MA, Allen JE et al. Highly evolvable malaria vectors: The genomes of 16 Anopheles mosquitoes. Science. 2015 Jan 2;347(6217). 1258522. https://doi.org/10.1126/science.1258522
Neafsey, Daniel E. ; Waterhouse, Robert M. ; Abai, Mohammad R. ; Aganezov, Sergey S. ; Alekseyev, Max A. ; Allen, James E. ; Amon, James ; Arcà, Bruno ; Arensburger, Peter ; Artemov, Gleb ; Assour, Lauren A. ; Basseri, Hamidreza ; Berlin, Aaron ; Birren, Bruce W. ; Blandin, Stephanie A. ; Brockman, Andrew I. ; Burkot, Thomas R. ; Burt, Austin ; Chan, Clara S. ; Chauve, Cedric ; Chiu, Joanna C. ; Christensen, Mikkel ; Costantini, Carlo ; Davidson, Victoria L M ; Deligianni, Elena ; Dottorini, Tania ; Dritsou, Vicky ; Gabriel, Stacey B. ; Guelbeogo, Wamdaogo M. ; Hall, Andrew B. ; Han, Mira V. ; Hlaing, Thaung ; Hughes, Daniel S T ; Jenkins, Adam M. ; Jiang, Xiaofang ; Jungreis, Irwin ; Kakani, Evdoxia G. ; Kamali, Maryam ; Kemppainen, Petri ; Kennedy, Ryan C. ; Kirmitzoglou, Ioannis K. ; Koekemoer, Lizette L. ; Laban, Njoroge ; Langridge, Nicholas ; Lawniczak, Mara K N ; Lirakis, Manolis ; Lobo, Neil F. ; Lowy, Ernesto ; MacCallum, Robert M. ; Mao, Chunhong ; Maslen, Gareth ; Mbogo, Charles ; McCarthy, Jenny ; Michel, Kristin ; Mitchell, Sara N. ; Moore, Wendy ; Murphy, Katherine A. ; Naumenko, Anastasia N. ; Nolan, Tony ; Novoa, Eva M. ; O'Loughlin, Samantha ; Oringanje, Chioma ; Oshaghi, Mohammad A. ; Pakpour, Nazzy ; Papathanos, Philippos A. ; Peery, Ashley N. ; Povelones, Michael ; Prakash, Anil ; Price, David P. ; Rajaraman, Ashok ; Reimer, Lisa J. ; Rinker, David C. ; Rokas, Antonis ; Russell, Tanya L. ; Sagnon, N'Fale ; Sharakhova, Maria V. ; Shea, Terrance ; Simão, Felipe A. ; Simard, Frederic ; Slotman, Michel A. ; Somboon, Pradya ; Stegniy, Vladimir ; Struchiner, Claudio J. ; Thomas, Gregg W C ; Tojo, Marta ; Topalis, Pantelis ; Tubio, José M C ; Unger, Maria F. ; Vontas, John ; Walton, Catherine ; Wilding, Craig S. ; Willis, Judith H. ; Wu, Yi Chieh ; Yan, Guiyun ; Zdobnov, Evgeny M. ; Zhou, Xiaofan ; Catteruccia, Flaminia ; Christophides, George K. ; Collins, Frank H. ; Cornman, Robert S. ; Crisanti, Andrea ; Donnelly, Martin J. ; Emrich, Scott J. ; Fontaine, Michael C. ; Gelbart, William ; Hahn, Matthew W. ; Hansen, Immo A. ; Howell, Paul I. ; Kafatos, Fotis C. ; Kellis, Manolis ; Lawson, Daniel ; Louis, Christos ; Luckhart, Shirley ; Muskavitch, Marc A T ; Ribeiro, José M. ; Riehle, Michael A. ; Sharakhov, Igor V. ; Tu, Zhijian ; Zwiebel, Laurence J. ; Besansky, Nora J. / Highly evolvable malaria vectors : The genomes of 16 Anopheles mosquitoes. In: Science. 2015 ; Vol. 347, No. 6217.
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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.",
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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

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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

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AU - Lowy, Ernesto

AU - MacCallum, Robert M.

AU - Mao, Chunhong

AU - Maslen, Gareth

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AU - Mitchell, Sara N.

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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.

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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 J.

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.

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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.

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