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Temperature drives transmission of mosquito-borne pathogens: improving entomological estimates for Aedes aegypti-borne virus transmission risk

Abstract

The mosquito Aedes aegypti is the primary vector of many viruses that cause a major burden on human health worldwide, including dengue, Zika, yellow fever, and chikungunya viruses. Currently, a widely adopted vaccine is available only for yellow fever virus, and thus mitigating the burden of diseases caused by these viruses predominantly relies on avoiding mosquito bites and controlling mosquito populations. Mosquito-borne virus transmission risk models can help mosquito control decision-makers efficiently use limited resources and reduce the use of chemical insecticides that can lead to resistance and therefore less effective control. As the Zika virus (ZIKV) pandemic emerged in 2016, estimates for ZIKV transmission risk were based on proxy evidence from closely related dengue virus. To improve risk estimates, we first studied how temperature affects ZIKV extrinsic incubation period (EIP). We concluded that, in agreement with findings for other mosquito-borne viruses, ZIKV EIP decreased as temperature increased and ZIKV EIP was relatively shorter than for dengue virus across temperatures. We then sought to further improve ZIKV risk estimates by studying thermal preferences of Ae. aegypti mosquitoes in the laboratory and in the field. Current mosquito-borne pathogen risk models primarily use temperatures from weather stations or thermal imagery as a proxy for the temperatures mosquitoes experience; however, such approaches do not account for the range of local environments or microclimates available to adult mosquitoes nor the microhabitats mosquitoes select and therefore may lead to an inaccurate estimate of risk. In the lab, Ae. aegypti generally preferred the coldest temperatures available (<20°C) and avoided the hottest temperatures (>31°C) on a gradient ranging from 17.5°C to 36.5°C. However, mosquitoes reared at cooler temperatures (22°C) were larger and rested at warmer temperatures compared to mosquitoes reared at warm temperatures (26°C and 30°C). In the field, female Ae. aegypti were found resting at temperatures that were increasingly cooler than ambient as ambient air temperature increased. Accordingly bias in air-temperature-based models of Zika virus transmission risk is expected to be greatest at the hottest temperatures, and overall, accounting for Ae. aegypti thermal preferences yielded lower estimates for Zika virus transmission risk compared to models based on air temperatures alone. Taken together, the results of these studies can be used to improve prediction of mosquito-borne pathogen risk and inform mosquito control decisions.

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