Impact of daily temperature fluctuations on dengue virus transmission by Aedes aegypti

Abstract

Most studies on the ability of insect populations to transmit pathogens consider only constant temperatures and do not account for realistic daily temperature fluctuations that can impact vector-pathogen interactions. Here, we show that diurnal temperature range (DTR) affects two important parameters underlying dengue virus (DENV) transmission by Aedes aegypti. In two independent experiments using different DENV serotypes, mosquitoes were less susceptible to virus infection and died faster under larger DTR around the same mean temperature. Large DTR (20 °C) decreased the probability of midgut infection, but not duration of the virus extrinsic incubation period (EIP), compared with moderate DTR (10 °C) or constant temperature. A thermodynamic model predicted that at mean temperatures <18 °C, DENV transmission increases as DTR increases, whereas at mean temperatures >18 °C, larger DTR reduces DENV transmission. The negative impact of DTR on Ae. aegypti survival indicates that large temperature fluctuations will reduce the probability of vector survival through EIP and expectation of infectious life. Seasonal variation in the amplitude of daily temperature fluctuations helps to explain seasonal forcing of DENV transmission at locations where average temperature does not vary seasonally and mosquito abundance is not associated with dengue incidence. Mosquitoes lived longer and were more likely to become infected under moderate temperature fluctuations, which is typical of the high DENV transmission season than under large temperature fluctuations, which is typical of the low DENV transmission season. Our findings reveal the importance of considering short-term temperature variations when studying DENV transmission dynamics.

Fig. 1.

Seasonal DTR differences associated with the intensity of natural DENV transmission. Representative time series of daily temperature fluctuations measured during the high DENV transmission season (red symbols) and the low DENV transmission season (blue symbols) at Mae Sot, Tak Province, Thailand. The average temperature over the entire period is 26.7 °C for the high transmission season and 26.1 °C for the low transmission season.

Fig. 2.

Effects of EIP and DTR on Ae. aegypti experimental vector competence for DENV. Time course of (A) the percentage of females with a midgut infection and (B) the percentage of infected (excluding uninfected) females with a disseminated infection as a function of DTR regimes in two independent experiments (Exp1 and Exp2). Each data point represents 25 females in Exp1 and 3–28 females (mean 16) in Exp2. Lines are the logistic fits of the data. Overall, DTR significantly influences the percentage of infected females (P < 0.0001) but not the percentage of females with a disseminated infection (P = 0.234).

Fig. 3.

Combined theoretical effects of mean temperature and DTR on Ae. aegypti vector competence for DENV. The probability (right-hand bar) that the virus (A) infects the mosquito and (B) is subsequently transmitted across a range of mean temperatures and diurnal temperature ranges according to vector competence models (Fig. S4) In both panels, temperature variation is described by combined sine and exponential functions (a sinusoidal progression during daytime and a decreasing exponential curve during the night).

Fig. 4.

Effect of DTR on experimental survival of Ae. aegypti females after oral exposure to DENV. Kaplan–Meier analysis of survival rates following exposure to an infectious blood meal as a function of diurnal temperature regimes. In A, mosquitoes were exposed to a DENV-2 isolate. Survival curves are significantly different according to log-rank tests (overall: P < 0.0001; DTR = 0 °C vs. DTR = 10 °C: P = 0.0249; DTR = 10 °C vs. DTR = 20 °C: P = 0.0068). In B, mosquitoes were exposed to a DENV-1 isolate. Survival curves are significantly different according to a log-rank test (P < 0.0001). Vertical bars indicate SE.