Carry-over effects of urban larval environments on the transmission potential of dengue-2 virus

Abstract

Background: Mosquitoes are strongly influenced by environmental temperatures, both directly and indirectly via carry-over effects, a phenomenon by which adult phenotypes are shaped indirectly by the environmental conditions experienced in previous life stages. In landscapes with spatially varying microclimates, such as a city, the effects of environmental temperature can therefore lead to spatial patterns in disease dynamics. To explore the contribution of carry-over effects on the transmission of dengue-2 virus (DENV-2), we conducted a semi-field experiment comparing the demographic and transmission rates of Aedes albopictus reared on different urban land classes in the summer and autumn season. We parameterized a model of vectorial capacity using field- and literature-derived measurements to estimate the bias introduced into predictions of vectorial capacity not accounting for carry-over effects. Results: The larval environment of different land classes and seasons significantly impacted mosquito life history traits. Larval development and survival rates were higher in the summer than the autumn, with no difference across land class. The effect of land class on adult body size differed across season, with suburban mosquitoes having the smallest wing length in the summer and the largest wing length in the autumn, when compared to other land classes. Infection and dissemination rates were higher in the autumn and on suburban and rural land classes compared to urban. Infectiousness did not differ across land class or season. We estimate that not accounting for carry-over effects can underestimate disease transmission potential in suburban and urban sites in the summer by up to 25%. Conclusions: Our findings demonstrate the potential of the larval environment to differentially impact stages of DENV-2 infection in Ae. albopictus mosquitoes via carry-over effects. Failure to account for carry-over effects of the larval environment in mechanistic models can lead to biased estimates of disease transmission potential at fine-scales in urban environments.