Abstract

The global population at risk from mosquito-borne diseases—including dengue, yellow fever, chikungunya and Zika—is expanding in concert with changes in the distribution of two key vectors: Aedes aegypti and Aedes albopictus. The distribution of these species is largely driven by both human movement and the presence of suitable climate. Using statistical mapping techniques, we show that human movement patterns explain the spread of both species in Europe and the United States following their introduction. We find that the spread of Ae. aegypti is characterized by long distance importations, while Ae. albopictus has expanded more along the fringes of its distribution. We describe these processes and predict the future distributions of both species in response to accelerating urbanization, connectivity and climate change. Global surveillance and control efforts that aim to mitigate the spread of chikungunya, dengue, yellow fever and Zika viruses must consider the so far unabated spread of these mosquitos. Our maps and predictions offer an opportunity to strategically target surveillance and control programmes and thereby augment efforts to reduce arbovirus burden in human populations globally.

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Change history

  • 21 March 2019

    In the version of this Article originally published, the affiliation for author Catherine Linard was incorrectly stated as ‘6Department of Infectious Disease Epidemiology, London School of Hygiene and Tropical Medicine, London, UK’. The correct affiliation is ‘9Spatial Epidemiology Lab (SpELL), Universite Libre de Bruxelles, Brussels, Belgium’. The affiliation for author Hongjie Yu was also incorrectly stated as ‘11Department of Statistics, Harvard University, Cambridge, MA, USA’. The correct affiliation is ‘15School of Health, Fudan University, Key Laboratory of Public Health Safety, Ministry of Education, Shanghai, China’. This has now been amended in all versions of the Article.

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Acknowledgements

The authors thank S. Ray for providing comments during the revision process. M.U.G.K. acknowledges funding from the Society in Science, The Branco Weiss Fellowship, administered by the ETH Zurich. M.U.G.K. also acknowledges funding from the Training Grant from the National Institute of Child Health and Human Development (T32HD040128). M.U.G.K., S.I.H., J.P.M., N.G., O.J.B. and G.R.W.W. acknowledge funding from the International Research Consortium on Dengue Risk Assessment Management and Surveillance (IDAMS; European Commission 7th Framework Programme no. 21893). O.B.J. was funded by a Sir Henry Wellcome Fellowship funded by the Wellcome Trust (grant number 206471/Z/17/Z) and a grant from the Bill and Melinda Gates Foundation (OP1183567). S.I.H. received a grant from the Research for Health in Humanitarian Crises (R2HC) Programme, managed by Enhancing Learning and Research for Humanitarian Assistance (ELRHA; no. 13468), which also supported M.U.G.K. and N.G. The R2HC programme aims to improve health outcomes by strengthening the evidence base for public health interventions in humanitarian crises. The £8 million R2HC programme is funded equally by the Wellcome Trust and Department of International Development (DFiD), with ELRHA overseeing the programme’s execution and management. S.I.H. was also funded by a Senior Research Fellowship from the Wellcome Trust (no. 95066) and grants from the Bill & Melinda Gates Foundation (OPP1106023, OPP1093011, OPP1132415 and OPP1159934). This study was made possible by the support of the American people through the US Agency for International Development Emerging Pandemic Threats Program-2 PREDICT-2 (Cooperative Agreement number AID-OAA-A-14-00102), which also supported M.U.G.K. J.S.B. is supported by the National Library of Medicine of the National Institutes of Health (R01LM010812 and R01LM011965), which also supports M.U.G.K. D.L.S. is funded by the National Institutes of Health and National Institute of Allergy and Infectious Diseases (no. U10AI089674). H.H.N. was funded by the European Commission through the European Research Council Advanced Investigator Grant ‘Momentum’ 324247. L.L. received funding from the French Government’s Investissement d’Avenir program, Laboratoire d’Excellence Integrative Biology of Emerging Infectious Diseases (grant ANR-10-LABX-62-IBEID), the French Agence Nationale de la Recherche (grant ANR-16-CE35-0004), the City of Paris Emergence(s) programme in Biomedical Research, and the European Union’s Horizon 2020 research and innovation programme under ZikaPLAN grant agreement No. 734584. S.C. received funding from the AXA Research Fund, the Investissement d’Avenir program, the Laboratoire d’Excellence Integrative Biology of Emerging Infectious Diseases program (Grant ANR-10-LABX-62-IBEID), the Models of Infectious Disease Agent Study of the National Institute of General Medical Sciences, the INCEPTION project (PIA/ANR-16-CONV-0005), and the European Union’s Horizon 2020 research and innovation programme under ZIKAlliance grant agreement No 734548. N.G. is supported by a University of Melbourne McKenzie fellowship. W.V.B., G.H. and F.S. acknowledge funding from VBORNET and VectorNet, an ECDC and EFSA-funded project (no. ECDC/09/018 and OC/EFSA/AHAW/2013/02), and thank all contributing VBORNET and VectorNet experts for data sharing. T.W.S., R.C.R. and L.L. received funding from the National Institutes of Health Program Project grant (no. P01 AI098670). X.L. is supported by the Natural Science Foundation of China (71771213, 71522014, 71725001, 91846301 and 71790615). This work was also partially supported by the European Union’s Horizon 2020 Research and Innovation Programme under ZIKAlliance Grant Agreement no. 734548.

Author information

Author notes

  1. These authors contributed equally: Moritz U. G. Kraemer, Robert C. Reiner Jr, Oliver J. Brady, Jane P. Messina, Marius Gilbert.

  2. These authors jointly supervised this work: Simon I. Hay, Nick Golding.

Affiliations

  1. Department of Zoology, University of Oxford, Oxford, UK

    • Moritz U. G. Kraemer
    • , Nuno R. Faria
    • , Oliver G. Pybus
    •  & G. R. William Wint
  2. Harvard Medical School, Harvard University, Boston, MA, USA

    • Moritz U. G. Kraemer
    •  & John S. Brownstein
  3. Boston Children’s Hospital, Boston, MA, USA

    • Moritz U. G. Kraemer
    •  & John S. Brownstein
  4. Institute for Health Metrics and Evaluation, University of Washington, Seattle, WA, USA

    • Robert C. Reiner Jr
    • , David M. Pigott
    • , Kimberly Johnson
    • , Lucas Earl
    • , Laurie B. Marczak
    • , Shreya Shirude
    • , Nicole Davis Weaver
    • , David L. Smith
    •  & Simon I. Hay
  5. Centre for Mathematical Modelling of Infectious Diseases, London School of Hygiene and Tropical Medicine, London, UK

    • Oliver J. Brady
  6. Department of Infectious Disease Epidemiology, London School of Hygiene and Tropical Medicine, London, UK

    • Oliver J. Brady
  7. School of Geography and the Environment, University of Oxford, Oxford, UK

    • Jane P. Messina
  8. Oxford School of Global and Area Studies, University of Oxford, Oxford, UK

    • Jane P. Messina
  9. Spatial Epidemiology Lab (SpELL), Universite Libre de Bruxelles, Brussels, Belgium

    • Marius Gilbert
    •  & Catherine Linard
  10. Fonds National de la Recherche Scientifique, Brussels, Belgium

    • Marius Gilbert
  11. Department of Statistics, Harvard University, Cambridge, MA, USA

    • Dingdong Yi
  12. RTI International, Washington, DC, USA

    • Donal Bisanzio
  13. Epidemiology and Public Health Division, School of Medicine, University of Nottingham, Nottingham, UK

    • Donal Bisanzio
  14. Department of Biological Sciences and Eck Institute for Global Health, University of Notre Dame, Notre Dame, IN, USA

    • T. Alex Perkins
  15. School of Health, Fudan University, Key Laboratory of Public Health Safety, Ministry of Education, Shanghai, China

    • Shengjie Lai
    •  & Hongjie Yu
  16. Department of Geography and Environment, University of Southampton, Southampton, UK

    • Shengjie Lai
    •  & Andrew J. Tatem
  17. Flowminder Foundation, Stockholm, Sweden

    • Shengjie Lai
    • , Linus Bengtsson
    • , Erik Wetter
    •  & Andrew J. Tatem
  18. School of Business, Central South University, Changsha, China

    • Xin Lu
  19. College of Systems Engineering, National University of Defense Technology, Changsha, China

    • Xin Lu
  20. School of Business Administration, Southwestern University of Finance and Economics, Chengdu, China

    • Xin Lu
  21. Waen Associates Ltd, Y Waen, Islaw’r Dref, Dolgellau, Gwynedd, UK

    • Peter Jones
  22. Pan American Health Organization (PAHO), Washington, DC, USA

    • Giovanini E. Coelho
  23. National Dengue Control Program, Ministry of Health, Brasilia, Brazil

    • Roberta G. Carvalho
  24. European Centre for Disease Prevention and Control, Stockholm, Sweden

    • Wim Van Bortel
  25. Institute of Tropical Medicine, Antwerp, Belgium

    • Wim Van Bortel
  26. Avia-GIS, Zoersel, Belgium

    • Cedric Marsboom
    •  & Guy Hendrickx
  27. Francis Schaffner Consultancy, Riehen, Switzerland

    • Francis Schaffner
  28. Department of Microbiology, Immunology, and Pathology, Colorado State University, Fort Collins, CO, USA

    • Chester G. Moore
  29. Computational Social Science, ETH Zurich, Zurich, Switzerland

    • Heinrich H. Nax
  30. Department of Public Health Sciences, Karolinska Institutet, Stockholm, Sweden

    • Linus Bengtsson
  31. Stockholm School of Economics, Stockholm, Sweden

    • Erik Wetter
  32. Insect–Virus Interactions Unit, Institut Pasteur, CNRS, UMR2000, Paris, France

    • Louis Lambrechts
  33. Mathematical Modelling of Infectious Diseases Unit, Institut Pasteur, CNRS, UMR2000, Paris, France

    • Simon Cauchemez
  34. Department of Geography, Universite de Namur, Namur, Belgium

    • Catherine Linard
  35. Department of Entomology and Nematology, University of California, Davis, Davis, CA, USA

    • Thomas W. Scott
  36. State Key Laboratory of Infectious Disease Prevention and Control, Collaborative Innovation Center for Diagnosis and Treatment of Infectious Diseases, National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Changping, Beijing, China

    • Qiyong Liu
  37. Shandong University Climate Change and Health Center, School of Public Health, Shandong University, Jinan, Shandong, China

    • Qiyong Liu
  38. WHO Collaborating Centre for Vector Surveillance and Management, Beijing, China

    • Qiyong Liu
  39. Chongqing Centre for Disease Control and Prevention, Chongqing, China

    • Qiyong Liu
  40. Environmental Research Group Oxford (ERGO), Department of Zoology, Oxford University, Oxford, UK

    • G. R. William Wint
  41. School of BioSciences, University of Melbourne, Parkville, Victoria, Australia

    • Nick Golding

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Contributions

All contributions are listed in the order of authorship. M.U.G.K., R.C.R., O.J.B., S.I.H. and N.G. designed the experiments. S.L., X.L., C.M., K.J., L.E., J.S.B., C.L., P.J., G.E.C., L.B., E.W., A.J.T., R.G.C., W.V.B., G.H., F.S., C.G.M., Q.L., G.R.W.W. and H.Y. provided data. M.U.G.K., R.C.R., O.J.B., J.P.M. and M.G. analysed the data. M.U.G.K., R.C.R., O.J.B., J.P.M., M.G., D.Y., D.B., T.A.P., H.H.N., D.L.S., L.L., S.C., N.R.F., O.G.P., T.W.S., G.R.W.W., S.I.H. and N.G. interpreted the results. J.P.M., L.B.M., S.S., N.D.W., D.M.P., G.R.W.W. and S.I.H. edited the manuscript. M.U.G.K., O.J.B., O.G.P., S.I.H. and N.G. wrote the manuscript. All authors read and approved the content of the manuscript.

Competing interest

The authors declare no competing interests.

Corresponding authors

Correspondence to Moritz U. G. Kraemer or Simon I. Hay or Nick Golding.

Supplementary information

  1. Supplementary Information

    Supplementary Notes, Supplementary Figures 1–13, Supplementary Tables 1–9 and Supplementary References.

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DOI

https://doi.org/10.1038/s41564-019-0376-y