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bioRxiv · 10.1101/2021.09.07.459140

How do I bite thee? Let me count the ways: Heterogeneity and temperature dependence in Ae. aegypti biting habits drive individual mosquito arbovirus transmission potential

Abstract

In models of mosquito-borne transmission, the mosquito biting rate is an influential parameter, and understanding the heterogeneity of the process of biting is important, as biting is usually assumed to be relatively homogeneous across individuals, with time-between-bites described by an exponentially distributed process. However, these assumptions have not been addressed through laboratory experimentation. We experimentally investigated the daily biting habits of Ae. aegypti at three temperatures (24{degrees}C, 28{degrees}C, and 32{degrees}C) and determined that there was individual heterogeneity in biting habits (number of bites, timing of bites, etc.). We further explored the consequences of biting heterogeneity using an individual-based model designed to examine whether a particular biting profile determines whether a mosquito is more or less likely to 1) become exposed given a single index case of dengue (DENV) and 2) transmit to a susceptible human individual. Our experimental results indicate that there is heterogeneity among individuals and among temperature treatments. We further show that this results in altered probabilities of transmission of DENV to and from individual mosquitoes based on biting profiles. While current model representation of biting may work under some conditions, it might not uniformly be the best fit for this process. Our data also confirm that biting is a non-monotonic process with temperatures around 28{degrees}C being optimum. Author SummaryMosquito biting is a necessary and critical part of arbovirus transmission. The mosquito must bite once to acquire a virus and again to transmit, and these two bites must be separated by sufficient time for the virus to get to the salivary glands of the mosquito. Thus, both the number and timing of bites is important. We experimentally investigated how these bite characteristics might be different among individuals and further explored how temperature affected the overall heterogeneity of biting in Aedes aegypti mosquitoes, which carry many arboviruses like dengue virus (DENV). We found that the biting profiles - including number and timing thereof - did vary within temperature groups among individuals and compared outcomes associated with each individual in an individual based model of household DENV transmission. Our results further confirmed that temperatures around 28{degrees}C are optimal for mosquito biting (and transmission), that correlations between biting characteristics and transmission were not uniform across temperature, which represents another layer of heterogeneity, and that - at least at 28{degrees}C - the null assumption of an exponential or an exponential like (geometric) distribution of biting in mathematical models of transmission is not the best and offer an alternative.

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Christofferson, R. C., Wearing, H. J., Walsh, C. E., Salje, H., Tran Kiem, C., Cauchemez, S.. 2021-09-08. How do I bite thee? Let me count the ways: Heterogeneity and temperature dependence in Ae. aegypti biting habits drive individual mosquito arbovirus transmission potential. https://doi.org/10.1101/2021.09.07.459140

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