Abstract

BackgroundEnvironmental 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 FindingsWe 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.ConclusionsOur 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.

Highlights

  • The ability of Aedes aegypti to transmit viruses, in particular dengue viruses (DENV), has long been known to be influenced by temperature [1,2,3,4,5,6]

  • Our results indicate that Ae. aegypti exposed to large fluctuations at low temperatures have a significantly shorter virus extrinsic incubation period (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

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Summary

Introduction

The ability of Aedes aegypti to transmit viruses, in particular dengue viruses (DENV), has long been known to be influenced by temperature [1,2,3,4,5,6]. Lower temperatures generally extend the duration of EIP [5,6,8]; at 21uC and below, the EIP for DENV can be in the order of several weeks [3,4]. Despite these prolonged incubation periods, DENV-infected Ae. aegypti are capable of transmitting virus under laboratory conditions after incubation at temperatures as low as 13uC [4], and can become infective after incubation under temperature as low as 10uC [8]. Evidence to support an upper thermal threshold for DENV transmission is more limited Environmental factors such as temperature can alter mosquito vector competence for arboviruses. Theoretical predictions suggest that the mean temperature in combination with the magnitude of the diurnal temperature range (DTR) mediate the direction of these effects

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