Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-25T07:36:23.440Z Has data issue: false hasContentIssue false
  • English
  • Français

Using evolutionary costs to enhance the efficacy of malaria control via genetically manipulated mosquitoes

Published online by Cambridge University Press:  24 January 2008

JACOB C. KOELLA  and
LAMIA ZAGHLOUL
JACOB C. KOELLA*
Affiliation:
Imperial College London, Silwood Park Campus, Ascot SL5 7PY, United Kingdom
LAMIA ZAGHLOUL
Affiliation:
Laboratoire Joliot-Curie, ENS Lyon, 46, allée d'Italie 69364 Lyon Cedex 07, France
*
*Corresponding author: Jacob Koella, Imperial College London, Silwood Park Campus, Ascot SL5 7PY, United Kingdom. Tel: +44 2070542254. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

An earlier mathematical model exploring the use of genetically manipulated mosquitoes for malaria control suggested that the prevalence of malaria is reduced significantly only if almost all mosquitoes become completely resistant to malaria. Central to the model was the ‘cost of resistance’: the reduction of a resistant mosquito's evolutionary fitness in comparison with a sensitive one's. Here, we consider the possibility of obtaining more optimistic outcomes by taking into account the epidemiological (in addition to the evolutionary) consequences of a cost of resistance that decreases the life-span of adult mosquitoes (the most relevant parameter for the parasite's epidemiology). There are two main results. First, if despite its cost, resistance is fixed in the population, increasing the cost of resistance decreases the intensity of transmission. However, this epidemiological effect is weak if resistance is effective enough to be considered relevant for control. Second, if the cost of resistance prevents its fixation, increasing it intensifies transmission. Thus, the epidemiological effect of the cost of resistance cannot compensate for the lower frequency of resistant mosquitoes in the population. Overall, our conclusion remains pessimistic: so that genetic manipulation can become a promising method of malaria control, we need techniques that enable almost all mosquitoes to be almost completely resistant to infection.

Keywords

malariaAnophelesgenetic manipulationcost of resistancemalaria control
Type
Research Article
Information
Parasitology , Volume 135 , Special Issue 13: Mathematical modelling of parasitic infections: from data and parameter estimation to evolutionary implications , November 2008 , pp. 1489 - 1496
Copyright
Copyright © 2008 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Beaty, B. J. (2000). Genetic manipulation of vectors: a potential novel approach for control of vector borne diseases. Proceedings of the National Academy of Sciences, USA 97, 10295–10297.Google Scholar
Boëte, C. and Koella, J. C. (2002). A theoretical approach to predicting the success of genetic manipulation of malaria mosquitoes in malaria control. Malaria Journal 1, 3.CrossRefGoogle ScholarPubMed
Boëte, C., Paul, R. E. L. and Koella, J. C. (2004). Direct and indirect immuno-suppression by a malaria parasite in its mosquito vector. Proceedings of the Royal Society B 271, 1611–1615.CrossRefGoogle Scholar
Catteruccia, F., Nolan, T., Loukeris, T. G., Blass, C., Savakis, C., Kafatos, F. C. and Crisanti, A. (2000). Stable germline transformation of the malaria mosquito Anopheles stephensi. Nature 405, 959–962.CrossRefGoogle ScholarPubMed
Chen, C.-H., Huang, H., Ward, C. M., Su, J. T., Schaeffer, L. V., Guo, M. and Hay, B. A. (2007). A synthetic maternal-effect selfish genetic element drives population replacement in Drosophila. Science 316, 597–600.CrossRefGoogle ScholarPubMed
Dimopoulos, G. (2003). Insect immunity and its implication in mosquito-malaria interactions. Cellular Microbiology 5, 3–14.CrossRefGoogle ScholarPubMed
Hartl, D. L. and Clark, A. G. (1989). Principles of Population Genetics, Sinauer Associates, Sunderland.Google Scholar
Hemingway, J., Field, L. and Vontas, J. (2002). An overview of insecticide resistance. Science 298, 96–97.CrossRefGoogle ScholarPubMed
Hurd, H., Taylor, P. J., Adams, D., Underhill, A. and Eggleston, P. (2005). Evaluating the costs of mosquito resistance to malaria parasites. Evolution 59, 2560–2572.Google ScholarPubMed
Hyde, J. E. (2005). Drug-resistant malaria. Trends in Parasitology 21, 494–498.Google Scholar
Ito, J., Ghosh, A., Moreira, L. A., Wimmer, E. A. and Jacobs-Lorena, M. (2002). Transgenic anopheline mosquitoes impaired in transmission of a malaria parasite. Nature 417, 452–455.CrossRefGoogle ScholarPubMed
Koella, J. C. and Boëte, C. (2003). A genetic correlation between age at pupation and melanisation immune response of the yellow fever mosquito Aedes aegypti. Evolution 56, 1074–1079.Google Scholar
Lobo, N. F., Clayton, J. R., Fraser, M. J., Kafatos, F. C. and Collins, F. H. (2006). High efficiency germ-line transformation of mosquitoes. Nature Protocols 1, 1312–1317.Google Scholar
Macdonald, G. (1957). The Epidemiology and Control of Malaria, Oxford University Press, London.Google Scholar
Marrelli, M. T., Li, C., Rasgon, J. L. and Jacobs-Lorena, M. (2007). Transgenic malaria-resistant mosquitoes have a fitness advantage when feeding on Plasmodium-infected blood. Proceedings of the National Academy of Sciences, USA 104, 5580–5583.CrossRefGoogle ScholarPubMed
Moreira, L. A., Ito, J., Ghosh, A., Devenporti, M., Zieler, H., Abraham, E. G., Crisanti, A., Nolan, T., Catterucia, F. and Jacobs-Lorena, M. (2002). Bee venom phospholipase inhibits malaria parasite development in transgenic mosquitoes. Journal of Biological Chemistry 277, 40839–40843.Google Scholar
Moreira, L. A., Wang, J., Collins, F. H. and Jacobs-Lorena, M. (2004). Fitness of Anopheline mosquitoes expressing transgenes that inhibit Plasmodium development. Genetics 166, 1337–1341.CrossRefGoogle ScholarPubMed
Moret, Y. and Schmid-Hempel, P. (2000). Survival for immunity: the price of immune system activation for bumblebee workers. Science 290, 1166–1168.Google Scholar
Schwartz, A. and Koella, J. C. (2004). The cost of immunity in the yellow fever mosquito, Aedes aegypti depends on the immune stimulus. Journal of Evolutionary Biology 17, 834–840.Google Scholar
Smith, D. L., McKenzie, F. E., Snow, R. W. and Hay, S. I. (2007). Revisiting the basic reproductive number for malaria and its implications for malaria control. PLoS Biology 5, e42.CrossRefGoogle ScholarPubMed
Takken, W. and Scott, T. W. (2003). Ecological Aspects for Application of Genetically Modified Mosquitoes, Kluwer Academic Publishers, Dordrecht.Google Scholar
WHO (2005). The World Malaria Report. http://rbm.who.int/wmr2005/.Google Scholar
Yan, G., Severson, D. W. and Christensen, B. M. (1997). Costs and benefits of mosquito refractoriness to malaria parasites: implications for genetic variability of mosquitoes and genetic control of malaria. Evolution 51, 441–450.Google Scholar