Temperature-dependent variation in the extrinsic incubation period elevates the risk of vector-borne disease emergence

Abstract

Identifying ecological drivers of disease transmission is central to understanding disease risks. For vector-borne diseases, temperature is a major determinant of transmission because vital parameters determining the fitness of parasites and vectors are highly temperature-sensitive, including the extrinsic incubation period required for parasites to develop within the vector. Temperature also underlies dramatic differences in the individual-level variation in the extrinsic incubation period, yet the influence of this variation in disease transmission is largely unexplored. We incorporate empirical estimates of dengue virus extrinsic incubation period and its variation across a range of temperatures into a stochastic model to examine the consequences for disease emergence. We find that such variation impacts the probability of disease emergence because exceptionally rapid, but empirically observed incubation — typically ignored by modelling only the average — increases the chance of disease emergence even at the limits of the temperature range for dengue transmission. We show that variation in the extrinsic incubation period causes the greatest proportional increase in the risk of disease emergence at cooler temperatures where the mean incubation period is long, and associated variation is large. Thus, ignoring EIP variation will likely lead to underestimation of the risk of vector-borne disease emergence in temperate climates.