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Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission

Nature volume 476, pages 454–457 (2011)Cite this article

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Abstract

Genetic manipulations of insect populations for pest control have been advocated for some time, but there are few cases where manipulated individuals have been released in the field and no cases where they have successfully invaded target populations1. Population transformation using the intracellular bacterium Wolbachia is particularly attractive because this maternally-inherited agent provides a powerful mechanism to invade natural populations through cytoplasmic incompatibility2. When Wolbachia are introduced into mosquitoes, they interfere with pathogen transmission and influence key life history traits such as lifespan3,4,5,6. Here we describe how the wMel Wolbachia infection, introduced into the dengue vector Aedes aegypti from Drosophila melanogaster7, successfully invaded two natural A. aegypti populations in Australia, reaching near-fixation in a few months following releases of wMel-infected A. aegypti adults. Models with plausible parameter values indicate that Wolbachia-infected mosquitoes suffered relatively small fitness costs, leading to an unstable equilibrium frequency <30% that must be exceeded for invasion. These findings demonstrate that Wolbachia-based strategies can be deployed as a practical approach to dengue suppression with potential for area-wide implementation.

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Figure 1: Number of mosquitoes released, timing of releases, and changes in infection frequencies over time.
Figure 2: Changes in frequencies of Wolbachia -infected mosquitoes.
Figure 3: Occurrence of Aedes aegypti and Wolbachia infection in ovitraps outside release areas.

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Acknowledgements

We are grateful to J. Sutton, C. Paton, G. Omodei, S. Long, A. Gofton, V. White, A. Weeks, A. James, J. Dick, R. Bagita, P. Gibson, J. Jeffery, E. Rances, D. Rossi and J. Gough for technical and mapping support. We thank B. Kay for ongoing advice. We acknowledge and thank both D. McNaughton and D. Eastop for the early community engagement work preceding the trial. We thank all of our volunteers who helped blood-feed the mosquito colonies and we are particularly grateful to the residents of Gordonvale and Yorkeys Knob for their strong support and participation. This research was supported by a grant from the Foundation for the National Institutes of Health through the Grand Challenges in Global Health Initiative of the Bill and Melinda Gates Foundation, The National Health and Medical Research Council, Australia, the National and International Research Alliances Program of the Queensland Government, the RAPIDD program of the NIH, the Climate Health Cluster of the CSIRO Flagship Collaboration Fund, the National Science Foundation and Fellowships from the Australian Research Council.

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Authors and Affiliations

  1. Department of Genetics, Bio21 Institute, The University of Melbourne, Victoria 3010, Australia,

    A. A. Hoffmann, J. Axford & A. G. Callahan

  2. School of Biological Sciences, The University of Queensland, Brisbane, 4072, Queensland, Australia

    B. L. Montgomery, J. Popovici, I. Iturbe-Ormaetxe, F. Muzzi, M. Greenfield, M. Durkan, Y. S. Leong, Y. Dong, H. Cook, N. Kenny, E. A. McGraw, P. A. Ryan & S. L. O’Neill

  3. School of Biological Sciences, Monash University, Victoria 3800, Australia ,

    J. Popovici, I. Iturbe-Ormaetxe, Y. Dong, N. Kenny, E. A. McGraw, P. A. Ryan & S. L. O’Neill

  4. School of Public Health and Tropical Medicine and Rehabilitative Sciences, James Cook University, Cairns, 4870, Queensland, Australia

    P. H. Johnson, C. Omodei & S. A. Ritchie

  5. Queensland Institute of Medical Research, Post Office Royal Brisbane Hospital, Brisbane, 4029, Queensland, Australia

    P. A. Ryan

  6. Department of Evolution and Ecology, University of California, Davis, 95616, California, USA

    M. Turelli

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Contributions

A.A.H. and S.L.O. provided oversight of the releases and drafted most of the paper. S.A.R. and B.L.M. provided knowledge of local mosquito populations and liaison with authorities. J.P., I.I.-O., Y.D. and Y.S.L. carried out the Wolbachia screening. P.H.J., C.O., J.A., N.K., E.A.M. and A.G.C. were responsible for mosquito culture and backcrossing. Field releases and monitoring collections were undertaken by F.M., M.G., M.D. and B.L.M. and coordinated by B.L.M. and P.A.R. M.T. developed models to interpret the results and A.A.H. interpreted data during the release. H.C., S.L.O., S.A.R., M.D. and P.A.R. were involved in community engagement and mapping. S.L.O. and I.I.-O. were responsible for gaining regulatory approvals for the releases.

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Correspondence to S. L. O’Neill.

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The authors declare no competing financial interests.

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Hoffmann, A., Montgomery, B., Popovici, J. et al. Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission. Nature 476, 454–457 (2011). https://doi.org/10.1038/nature10356

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