Exposure to cooler temperatures during pupal development increases Aedes aegypti vector competence and the R0 for Zika virus

Abstract

Temperature profoundly affects various aspects of ectotherm biology. Notably, in mosquito species that spread viral diseases, temperature influences not only vector biology, but also the dynamics of pathogen-vector interactions. However, research attempting to address the role of the thermal environment in disease transmission often employs constant temperatures, which do not reflect the natural diurnal fluctuations these organisms experience. Additionally, most studies focus on adult mosquitoes in the period following virus infection. Much less attention has been paid to evidence indicating that temperatures experienced during earlier developmental stages may also affect the ability of disease vectors to be infected with and transmit viruses. Here, we show that Aedes aegypti exposed to temperatures below 25{degrees}C, specifically during the pupal stage of development, exhibit heightened susceptibility to Zika virus (ZIKV), which increases transmission efficiency. Modeling suggests that exposing mosquitoes to cooler fluctuating diurnal temperature ranges only during the relatively short pupal stage increases the R0 or reproductive number of ZIKV. Data loggers placed near Harris County Mosquito Control trap sites consistently recorded temperatures below 25{degrees}C, indicating natural exposure to such conditions. These results highlight the significance of thermal heterogeneity in the microhabitats where container-breeding mosquitoes undergo development. Such heterogeneity may play a more important role in the transmission of mosquito-borne diseases than previously recognized. Author SummaryA paucity of information regarding how natural heterogeneity in thermal environments influences the spread of viral pathogens by mosquito species hinders our ability to decipher current and future patterns of disease transmission under changing climatic conditions. Here, we show that Ae. aegypti pupae exposed to cooler fluctuating diurnal temperature ranges, mimicking realistic field conditions, increases vector competence for ZIKV. Modeling cooler temperatures during immature life stages predicts slower development and increased mortality, counterbalancing increases in disease transmission. However, exposing mosquitoes to lower temperatures only during the relatively short pupal stage was predicted to increase the R0 value of ZIKV. These results suggest that environmental temperatures specifically experienced during the pupal stage may have an important role in disease transmission.