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The influence of feeding behaviour and temperature on the capacity of mosquitoes to transmit malaria

Abstract

Insecticide-treated bed nets reduce malaria transmission by limiting contact between mosquito vectors and human hosts when mosquitoes feed during the night. However, malaria vectors can also feed in the early evening and in the morning when people are not protected. Here, we explored how the timing of blood feeding interacts with environmental temperature to influence the capacity of Anopheles mosquitoes to transmit the human malaria parasite Plasmodium falciparum. In laboratory experiments, we found no effect of biting time itself on the proportion of mosquitoes that became infectious (vector competence) at constant temperature. However, when mosquitoes were maintained under more realistic fluctuating temperatures, there was a significant increase in competence for mosquitoes feeding in the evening (18:00), and a significant reduction in competence for those feeding in the morning (06:00), relative to those feeding at midnight (00:00). These effects appear to be due to thermal sensitivity of malaria parasites during the initial stages of parasite development within the mosquito, and the fact that mosquitoes feeding in the evening experience cooling temperatures during the night, whereas mosquitoes feeding in the morning quickly experience warming temperatures that are inhibitory to parasite establishment. A transmission dynamics model illustrates that such differences in competence could have important implications for malaria prevalence, the extent of transmission that persists in the presence of bed nets, and the epidemiological impact of behavioural resistance. These results indicate that the interaction of temperature and feeding behaviour could be a major ecological determinant of the vectorial capacity of malaria mosquitoes.

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Fig. 1: Effects of the time of day of the blood meal and diurnal temperature fluctuation on the vector competence of A. gambiae mosquitoes infected with P. falciparum malaria.
Fig. 2: Model outputs illustrating the potential epidemiological significance of altered vector competence arising from biting time.
Fig. 3: Effect of exposure to high temperatures on vector competence of Anopheles mosquitoes infected with P. falciparum malaria.
Fig. 4: Behavioural assay to investigate thermal avoidance behaviour of A. gambiae mosquitoes following a blood meal.

Data availability

The raw data that support the findings of this study are available in Dryad with the identifier b2rbnzsb5 (ref. 93).

Code availability

The code used for modelling in this study is available at https://github.com/jamiegriffin/Malaria_simulation. Any changes to this code are described within this paper.

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Acknowledgements

We thank D. C. Soergel, J. L. Teeple and F. Ware-Gilmore for technical assistance, and D. A. Kennedy, E. D. Sternberg and L. Ge for advice on statistical analyses. This study was supported by NIH NIAID grant R01AI110793 and National Science Foundation Ecology and Evolution of Infectious Diseases grant DEB-1518681. The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.

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E.S., J.L.W., E.S.-S., T.S.C. and M.B.T. designed the research. E.S., J.L.W., N.L.D. and E.S.-S. performed the research. E.S., M.K.G., E.S.-S. and T.S.C. analysed the data. E.S., E.S.-S., T.S.C. and M.B.T. wrote the manuscript with input from M.K.G., J.L.W. and N.L.D.

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Correspondence to Eunho Suh.

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Suh, E., Grossman, M.K., Waite, J.L. et al. The influence of feeding behaviour and temperature on the capacity of mosquitoes to transmit malaria. Nat Ecol Evol 4, 940–951 (2020). https://doi.org/10.1038/s41559-020-1182-x

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