The tortoise strategy as an arbovirus fitness phenotype within the mosquito as revealed by a novel formulation of age-structured vectorial capacity

Abstract

The transmission of vector-borne diseases like Zika virus (ZIKV) is a dynamic process that is defined by intrinsic and extrinsic factors. One of the most important definers of the efficiency of the transmission is vector competence, or the ability of a vector to become infected with and eventually transmit a pathogen. Many things affect vector competence including vector species, discrete populations within species, and environmental factors. Several recent studies have focused on environmental factors such as temperature, and found that temperature not only affects vector competence of ZIKV in Aedes aegypti but also the life traits of the mosquito. Thus, we wanted to determine if the vector competence and extrinsic incubation period (EIP) of ZIKV was altered due to the age at which a mosquito becomes exposed. We found that there were virtually no differences in the proportion of infected, disseminated, or transmitting mosquitoes 5, 8, and 11 days post exposure among those mosquitoes exposed at 5 days post emergence versus those exposed at 12 days post emergence. However, to put this lack of differences into a more biologically relevant context, we investigated the interaction of vector competence, EIP, and age-dependent life traits of lifespan and biting rate. To illustrate the differences, we modified the vectorial capacity (VC) equation, which is a vector-centric equivalent to the basic reproduction number. VC describes the number of secondary cases of vector infection given the introduction of an infectious individual into a naïve population. By deriving an age-structure measure (VC age ), we are able to demonstrate the effect of age on the transmission of ZIKV by Ae. aegypti. While aging of mosquitoes in the field is limited to pre-parous and parous females, our VC age equation, like age-structured mathematical models, can be used to inform hypothesis regarding the effective density of mosquito vectors, those that are transmitting versus those that are unexposed or exposed but not transmitting due to the effects of age. These results are intuitive. However, our VC age model, like other models with age-structured vector populations, can be used to put this intuition into a quantitative framework and our experimental findings offer more insights into the importance of age-dependence of virus:vector interactions. Our experimental data further offer age-dependent parameterization of several components of VC age that could be used to inform mathematical models where age structure in a mosquito population is important.

Exposure to Zika and chikungunya viruses impacts aspects of the vectorial capacity ofAedes aegyptiandCulex quinquefasciatus

“…Significant changes in reproductive capacity, for example, can limit the number of offspring of infected females and determine the transmission dynamics of an arbovirus. In general, this dynamic also occurs as a function of the age at which the vector acquires the infection, as well as survival and longevity [5,6,45].…”

“…This has evolutionary implications, once any trait that may offer an adaptive advantage for the mosquito's defense against viral infection is unlikely to be selected for. However, the ability of a vector to transmit a pathogen is multifactorial and, therefore, isolated assessments in any of its parameters must be made with caution [45].…”