Fluctuations at a Low Mean Temperature Accelerate Dengue Virus Transmission by Aedes aegypti

Abstract

Environmental factors such as temperature can alter mosquito vector competence for arboviruses. Results from recent studies indicate that daily fluctuations around an intermediate mean temperature (26°C) reduce vector competence of Aedes aeygpti for dengue viruses (DENV). Theoretical predictions suggest that the mean temperature in combination with the magnitude of the diurnal temperature range (DTR) mediate the direction of these effects. We tested the effect of temperature fluctuations on Ae. aegypti vector competence for DENV serotype-1 at high and low mean temperatures, and confirmed this theoretical prediction. A small DTR had no effect on vector competence around a high (30°C) mean, but a large DTR at low temperature (20°C) increased the proportion of infected mosquitoes with a disseminated infection by 60% at 21 and 28 days post-exposure compared to a constant 20°C. This effect resulted from a marked shortening of DENV extrinsic incubation period (EIP) in its mosquito vector; i.e., a decrease from 29.6 to 18.9 days under the fluctuating vs. constant temperature treatment. Our results indicate that Ae. aegypti exposed to large fluctuations at low temperatures have a significantly shorter virus EIP than under constant temperature conditions at the same mean, leading to a considerably greater potential for DENV transmission. These results emphasize the value of accounting for daily temperature variation in an effort to more accurately understand and predict the risk of mosquito-borne pathogen transmission, provide a mechanism for sustained DENV transmission in endemic areas during cooler times of the year, and indicate that DENV transmission could be more efficient in temperate regions than previously anticipated. Mosquitoes in the wild are exposed to daily fluctuations in temperature, but in the laboratory, the effect of temperature on vector competence is generally assessed using constant temperatures. Recent studies demonstrate that realistic fluctuations in temperature around an intermediate mean (26°C) can alter life-history traits, population dynamics, and the ability of a mosquito to become infected with and transmit dengue virus (DENV). Here we tested how fluctuations around high and low mean temperatures influence vector competence and the extrinsic incubation period. Small fluctuations around a high mean temperature (∼8°C swings around 30°C) had no detectable effect on vector competence. Large fluctuations around a low mean (∼18°C swings around 20°C) demonstrate that only 18.9 days were required for 50% of DENV-exposed mosquitoes to develop a disseminated infection, compared to 29.6 days at constant 20°C. Twenty-eight days post-exposure to the infectious blood meal, 100% of mosquitoes tested had a disseminated infection under fluctuating temperatures, but under a constant temperature this proportion was only 42%. Reduced duration of extrinsic incubation increases the potential for pathogen transmission. Results indicate that the rate of dengue transmission by mosquitoes in temperate regions with natural fluctuations may be underestimated by experiments conducted under constant temperatures.