Mosquito genomics. 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 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

doi:10.1126/science.1258522

Mosquito genomics. Highly evolvable malaria vectors: the genomes of 16 Anopheles mosquitoes

Science. 2015 Jan 2;347(6217):1258522. doi: 10.1126/science.1258522. Epub 2014 Nov 27.

Authors

Daniel E Neafsey¹, Robert M Waterhouse², Mohammad R Abai³, Sergey S Aganezov⁴, Max A Alekseyev⁴, James E Allen⁵, James Amon⁶, Bruno Arcà⁷, Peter Arensburger⁸, Gleb Artemov⁹, Lauren A Assour¹⁰, Hamidreza Basseri³, Aaron Berlin¹¹, Bruce W Birren¹¹, Stephanie A Blandin¹², Andrew I Brockman¹³, Thomas R Burkot¹⁴, Austin Burt¹⁵, Clara S Chan¹⁶, Cedric Chauve¹⁷, Joanna C Chiu¹⁸, Mikkel Christensen⁵, Carlo Costantini¹⁹, Victoria L M Davidson²⁰, Elena Deligianni²¹, Tania Dottorini¹³, Vicky Dritsou²², Stacey B Gabriel²³, Wamdaogo M Guelbeogo²⁴, Andrew B Hall²⁵, Mira V Han²⁶, Thaung Hlaing²⁷, Daniel S T Hughes²⁸, Adam M Jenkins²⁹, Xiaofang Jiang³⁰, Irwin Jungreis¹⁶, Evdoxia G Kakani³¹, Maryam Kamali³², Petri Kemppainen³³, Ryan C Kennedy³⁴, Ioannis K Kirmitzoglou³⁵, Lizette L Koekemoer³⁶, Njoroge Laban³⁷, Nicholas Langridge⁵, Mara K N Lawniczak¹³, Manolis Lirakis³⁸, Neil F Lobo³⁹, Ernesto Lowy⁵, Robert M MacCallum¹³, Chunhong Mao⁴⁰, Gareth Maslen⁵, Charles Mbogo⁴¹, Jenny McCarthy⁸, Kristin Michel²⁰, Sara N Mitchell⁴², Wendy Moore⁴³, Katherine A Murphy¹⁸, Anastasia N Naumenko³², Tony Nolan¹³, Eva M Novoa¹⁶, Samantha O'Loughlin¹⁵, Chioma Oringanje⁴³, Mohammad A Oshaghi³, Nazzy Pakpour⁴⁴, Philippos A Papathanos⁴⁵, Ashley N Peery³², Michael Povelones⁴⁶, Anil Prakash⁴⁷, David P Price⁴⁸, Ashok Rajaraman¹⁷, Lisa J Reimer⁴⁹, David C Rinker⁵⁰, Antonis Rokas⁵¹, Tanya L Russell¹⁴, N'Fale Sagnon²⁴, Maria V Sharakhova³², Terrance Shea¹¹, Felipe A Simão⁵², Frederic Simard¹⁹, Michel A Slotman⁵³, Pradya Somboon⁵⁴, Vladimir Stegniy⁹, Claudio J Struchiner⁵⁵, Gregg W C Thomas⁵⁶, Marta Tojo⁵⁷, Pantelis Topalis²¹, José M C Tubio⁵⁸, Maria F Unger³⁹, John Vontas³⁸, Catherine Walton³³, Craig S Wilding⁵⁹, Judith H Willis⁶⁰, Yi-Chieh Wu⁶¹, Guiyun Yan⁶², Evgeny M Zdobnov⁵², Xiaofan Zhou⁶³, Flaminia Catteruccia³¹, George K Christophides¹³, Frank H Collins³⁹, Robert S Cornman⁶⁰, Andrea Crisanti⁴⁵, Martin J Donnelly⁶⁴, Scott J Emrich¹⁰, Michael C Fontaine⁶⁵, William Gelbart⁶⁶, Matthew W Hahn⁶⁷, Immo A Hansen⁴⁸, Paul I Howell⁶⁸, Fotis C Kafatos¹³, Manolis Kellis¹⁶, Daniel Lawson⁵, Christos Louis⁶⁹, Shirley Luckhart⁴⁴, Marc A T Muskavitch⁷⁰, José M Ribeiro⁷¹, Michael A Riehle⁴³, Igor V Sharakhov⁷², Zhijian Tu⁷³, Laurence J Zwiebel⁷⁴, Nora J Besansky⁷⁵

Affiliations

¹ Genome Sequencing and Analysis Program, Broad Institute, 415 Main Street, Cambridge, MA 02142, USA. neafsey@broadinstitute.org nbesansk@nd.edu.
² Computer Science and Artificial Intelligence Laboratory, Massachusetts Institute of Technology, 32 Vassar Street, Cambridge, MA 02139, USA. The Broad Institute of Massachusetts Institute of Technology and Harvard, 415 Main Street, Cambridge, MA 02142, USA. Department of Genetic Medicine and Development, University of Geneva Medical School, Rue Michel-Servet 1, 1211 Geneva, Switzerland. Swiss Institute of Bioinformatics, Rue Michel-Servet 1, 1211 Geneva, Switzerland.
³ Department of Medical Entomology and Vector Control, School of Public Health and Institute of Health Researches, Tehran University of Medical Sciences, Tehran, Iran.
⁴ George Washington University, Department of Mathematics and Computational Biology Institute, 45085 University Drive, Ashburn, VA 20147, USA.
⁵ European Molecular Biology Laboratory, European Bioinformatics Institute, EMBL-EBI, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SD, UK.
⁶ National Vector Borne Disease Control Programme, Ministry of Health, Tafea Province, Vanuatu.
⁷ Department of Public Health and Infectious Diseases, Division of Parasitology, Sapienza University of Rome, Piazzale Aldo Moro 5, 00185 Rome, Italy.
⁸ Department of Biological Sciences, California State Polytechnic-Pomona, 3801 West Temple Avenue, Pomona, CA 91768, USA.
⁹ Tomsk State University, 36 Lenina Avenue, Tomsk, Russia.
¹⁰ Department of Computer Science and Engineering, Eck Institute for Global Health, 211B Cushing Hall, University of Notre Dame, Notre Dame, IN 46556, USA.
¹¹ Genome Sequencing and Analysis Program, Broad Institute, 415 Main Street, Cambridge, MA 02142, USA.
¹² Inserm, U963, F-67084 Strasbourg, France. CNRS, UPR9022, IBMC, F-67084 Strasbourg, France.
¹³ Department of Life Sciences, Imperial College London, South Kensington Campus, London SW7 2AZ, UK.
¹⁴ Faculty of Medicine, Health and Molecular Science, Australian Institute of Tropical Health Medicine, James Cook University, Cairns 4870, Australia.
¹⁵ Department of Life Sciences, Imperial College London, Silwood Park Campus, Ascot SL5 7PY, UK.
¹⁶ Computer Science and Artificial Intelligence Laboratory, Massachusetts Institute of Technology, 32 Vassar Street, Cambridge, MA 02139, USA. The Broad Institute of Massachusetts Institute of Technology and Harvard, 415 Main Street, Cambridge, MA 02142, USA.
¹⁷ Department of Mathematics, Simon Fraser University, 8888 University Drive, Burnaby, BC V5A 1S6, Canada.
¹⁸ Department of Entomology and Nematology, One Shields Avenue, University of California-Davis, Davis, CA 95616, USA.
¹⁹ Institut de Recherche pour le Développement, Unités Mixtes de Recherche Maladies Infectieuses et Vecteurs Écologie, Génétique, Évolution et Contrôle, 911, Avenue Agropolis, BP 64501 Montpellier, France.
²⁰ Division of Biology, Kansas State University, 271 Chalmers Hall, Manhattan, KS 66506, USA.
²¹ Institute of Molecular Biology and Biotechnology, Foundation for Research and Technology, Hellas, Nikolaou Plastira 100 GR-70013, Heraklion, Crete, Greece.
²² Centre of Functional Genomics, University of Perugia, Perugia, Italy.
²³ Genomics Platform, Broad Institute, 415 Main Street, Cambridge, MA 02142, USA.
²⁴ Centre National de Recherche et de Formation sur le Paludisme, Ouagadougou 01 BP 2208, Burkina Faso.
²⁵ Program of Genetics, Bioinformatics, and Computational Biology, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061, USA.
²⁶ School of Life Sciences, University of Nevada, Las Vegas, NV 89154, USA.
²⁷ Department of Medical Research, No. 5 Ziwaka Road, Dagon Township, Yangon 11191, Myanmar.
²⁸ European Molecular Biology Laboratory, European Bioinformatics Institute, EMBL-EBI, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SD, UK. Baylor College of Medicine, 1 Baylor Plaza, Houston, TX 77030, USA.
²⁹ Boston College, 140 Commonwealth Avenue, Chestnut Hill, MA 02467, USA.
³⁰ Department of Biochemistry, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061, USA. Program of Genetics, Bioinformatics, and Computational Biology, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061, USA.
³¹ Harvard School of Public Health, Department of Immunology and Infectious Diseases, Boston, MA 02115, USA. Dipartimento di Medicina Sperimentale e Scienze Biochimiche, Università degli Studi di Perugia, Perugia, Italy.
³² Department of Entomology, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061, USA.
³³ Computational Evolutionary Biology Group, Faculty of Life Sciences, University of Manchester, Oxford Road, Manchester M13 9PT, UK.
³⁴ Department of Bioengineering and Therapeutic Sciences, University of California, San Francisco, CA 94143, USA.
³⁵ Department of Life Sciences, Imperial College London, South Kensington Campus, London SW7 2AZ, UK. Bioinformatics Research Laboratory, Department of Biological Sciences, New Campus, University of Cyprus, CY 1678 Nicosia, Cyprus.
³⁶ Wits Research Institute for Malaria, Faculty of Health Sciences, and Vector Control Reference Unit, National Institute for Communicable Diseases of the National Health Laboratory Service, Sandringham 2131, Johannesburg, South Africa.
³⁷ National Museums of Kenya, P.O. Box 40658-00100, Nairobi, Kenya.
³⁸ Department of Biology, University of Crete, 700 13 Heraklion, Greece.
³⁹ Eck Institute for Global Health and Department of Biological Sciences, University of Notre Dame, 317 Galvin Life Sciences Building, Notre Dame, IN 46556, USA.
⁴⁰ Virginia Bioinformatics Institute, 1015 Life Science Circle, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061, USA.
⁴¹ Kenya Medical Research Institute-Wellcome Trust Research Programme, Centre for Geographic Medicine Research - Coast, P.O. Box 230-80108, Kilifi, Kenya.
⁴² Harvard School of Public Health, Department of Immunology and Infectious Diseases, Boston, MA 02115, USA.
⁴³ Department of Entomology, 1140 East South Campus Drive, Forbes 410, University of Arizona, Tucson, AZ 85721, USA.
⁴⁴ Department of Medical Microbiology and Immunology, School of Medicine, University of California Davis, One Shields Avenue, Davis, CA 95616, USA.
⁴⁵ Department of Life Sciences, Imperial College London, South Kensington Campus, London SW7 2AZ, UK. Centre of Functional Genomics, University of Perugia, Perugia, Italy.
⁴⁶ Department of Pathobiology, University of Pennsylvania School of Veterinary Medicine, 3800 Spruce Street, Philadelphia, PA 19104, USA.
⁴⁷ Regional Medical Research Centre NE, Indian Council of Medical Research, P.O. Box 105, Dibrugarh-786 001, Assam, India.
⁴⁸ Department of Biology, New Mexico State University, Las Cruces, NM 88003, USA. Molecular Biology Program, New Mexico State University, Las Cruces, NM 88003, USA.
⁴⁹ Department of Vector Biology, Liverpool School of Tropical Medicine, Pembroke Place, Liverpool, L3 5QA, UK.
⁵⁰ Center for Human Genetics Research, Vanderbilt University Medical Center, Nashville, TN 37235, USA.
⁵¹ Center for Human Genetics Research, Vanderbilt University Medical Center, Nashville, TN 37235, USA. Department of Biological Sciences, Vanderbilt University, Nashville, TN 37235, USA.
⁵² Department of Genetic Medicine and Development, University of Geneva Medical School, Rue Michel-Servet 1, 1211 Geneva, Switzerland. Swiss Institute of Bioinformatics, Rue Michel-Servet 1, 1211 Geneva, Switzerland.
⁵³ Department of Entomology, Texas A&M University, College Station, TX 77807, USA.
⁵⁴ Department of Parasitology, Faculty of Medicine, Chiang Mai University, Chiang Mai 50200, Thailand.
⁵⁵ Fundação Oswaldo Cruz, Avenida Brasil 4365, RJ Brazil. Instituto de Medicina Social, Universidade do Estado do Rio de Janeiro, Rio de Janeiro, Brazil.
⁵⁶ School of Informatics and Computing, Indiana University, Bloomington, IN 47405, USA.
⁵⁷ Department of Physiology, School of Medicine, Center for Research in Molecular Medicine and Chronic Diseases, Instituto de Investigaciones Sanitarias, University of Santiago de Compostela, Santiago de Compostela, A Coruña, Spain.
⁵⁸ Wellcome Trust Sanger Institute, Hinxton, Cambridgeshire, CB10 1SA, UK.
⁵⁹ School of Natural Sciences and Psychology, Liverpool John Moores University, Liverpool L3 3AF, UK.
⁶⁰ Department of Cellular Biology, University of Georgia, Athens, GA 30602, USA.
⁶¹ Computer Science and Artificial Intelligence Laboratory, Massachusetts Institute of Technology, 32 Vassar Street, Cambridge, MA 02139, USA. The Broad Institute of Massachusetts Institute of Technology and Harvard, 415 Main Street, Cambridge, MA 02142, USA. Department of Computer Science, Harvey Mudd College, Claremont, CA 91711, USA.
⁶² Program in Public Health, College of Health Sciences, University of California, Irvine, Hewitt Hall, Irvine, CA 92697, USA.
⁶³ Department of Biological Sciences, Vanderbilt University, Nashville, TN 37235, USA.
⁶⁴ Department of Vector Biology, Liverpool School of Tropical Medicine, Pembroke Place, Liverpool, L3 5QA, UK. Malaria Programme, Wellcome Trust Sanger Institute, Cambridge CB10 1SJ, UK.
⁶⁵ Eck Institute for Global Health and Department of Biological Sciences, University of Notre Dame, 317 Galvin Life Sciences Building, Notre Dame, IN 46556, USA. Centre of Evolutionary and Ecological Studies (Marine Evolution and Conservation group), University of Groningen, Nijenborgh 7, NL-9747 AG Groningen, Netherlands.
⁶⁶ Department of Molecular and Cellular Biology, Harvard University, 16 Divinity Avenue, Cambridge, MA 02138, USA.
⁶⁷ Department of Biology, Indiana University, Bloomington, IN 47405, USA. School of Informatics and Computing, Indiana University, Bloomington, IN 47405, USA.
⁶⁸ Centers for Disease Control and Prevention, 1600 Clifton Road NE MSG49, Atlanta, GA 30329, USA.
⁶⁹ Department of Biology, University of Crete, 700 13 Heraklion, Greece. Institute of Molecular Biology and Biotechnology, Foundation for Research and Technology, Hellas, Nikolaou Plastira 100 GR-70013, Heraklion, Crete, Greece. Centre of Functional Genomics, University of Perugia, Perugia, Italy.
⁷⁰ Boston College, 140 Commonwealth Avenue, Chestnut Hill, MA 02467, USA. Biogen Idec, 14 Cambridge Center, Cambridge, MA 02142, USA.
⁷¹ Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases, 12735 Twinbrook Parkway, Rockville, MD 20852, USA.
⁷² Department of Entomology, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061, USA. Program of Genetics, Bioinformatics, and Computational Biology, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061, USA.
⁷³ Program of Genetics, Bioinformatics, and Computational Biology, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061, USA. Department of Biochemistry, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061, USA.
⁷⁴ Departments of Biological Sciences and Pharmacology, Institutes for Chemical Biology, Genetics and Global Health, Vanderbilt University and Medical Center, Nashville, TN 37235, USA.
⁷⁵ Eck Institute for Global Health and Department of Biological Sciences, University of Notre Dame, 317 Galvin Life Sciences Building, Notre Dame, IN 46556, USA. neafsey@broadinstitute.org nbesansk@nd.edu.

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.

Publication types

Research Support, N.I.H., Extramural

MeSH terms

Animals
Anopheles / classification
Anopheles / genetics*
Base Sequence
Chromosomes, Insect / genetics
Drosophila / genetics
Evolution, Molecular*
Genome, Insect*
Humans
Insect Vectors / classification
Insect Vectors / genetics*
Malaria / transmission*
Molecular Sequence Data
Phylogeny
Sequence Alignment

Associated data

BioProject/PRJNA67511

Abstract

Publication types

MeSH terms

Associated data

Grants and funding