Fluctuations at a low mean temperature accelerate dengue virus transmission by Aedes aegypti

Abstract

Background: 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.

Methodology/principal findings: 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.

Conclusions: 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.

Figure 1. Proportion of Ae. aegypti with a detectable infection after being held at low temperatures.

Females were held at 16°C, 20°C and 26°C constant, and 20°C with a large DTR and sampled at days 7, 14, 21 and 28 post-exposure to an infectious DENV-1 blood meal. A) Body infection, representing a detectable infection of the midgut tissue. B) Levels of infection in head tissue, representing a detectable disseminated infection.

Figure 2. Proportion of Ae. aegypti with a detectable infection after being held at high temperatures.

Females were held at 30°C and 35°C constant, and 30°C with a small DTR and sampled at days 3, 6 and 9 post-exposure to an infectious DENV-1 blood meal. A) Body infection, representing a detectable infection of the midgut tissue. B) Levels of infection in head tissue, representing a detectable disseminated infection.

Figure 3. Survival of females exposed to DENV-1 from various constant and cyclic temperature regimes.

A) Females held at low temperatures and a 26°C control. Despite the overall effect of temperature (p<0.0001), there were no differences in the survival curves after 28 days, between any of the three low temperature treatments (p>0.7). At 26°C constant, mortality was greater than in each of the low temperature treatments (p<0.001). B) Females held at high temperatures. Temperature influenced overall survival curves (p = 0.006), but only the curves of 30°C plus small DTR and 35°C constant were statistically different from each other (p = 0.001).