Dose and time-dependent chikungunya virus intra-vector dynamics in French Aedes albopictus mosquitoes highlights weak vector barriers leading to an explosive epidemic potential
Résumé
Arbovirus emergence and spread potential, as approximated by the vectorial capacity formula, depends on both host and vector parameters. Such parameters, shaped by biotic (e.g. genetic, microbial) and abiotic (e.g. temperature) factors, are intrinsically dynamic, thereby complicating their measurement. Although often evaluated as a qualitative phenotype, vector competence is a multistep, time-dependent, quantitative phenotype for which the dynamics is difficult to grasp. The combination of experimental and modeling approaches allows to i) capture intra-vector dynamics of arboviral infection and ii) estimate arbovirus epidemic potential upon a range of biotic/abiotic treatments. Here, we measured the proportion of individual Aedes albopictus mosquitoes from a French (Lyon) population that were infected by, disseminated, and transmitted chikungunya virus (CHIKV) at eleven time-points from day 2 to day 20 post-exposure (dpe) for a range of CHIKV infectious doses spanning human viremia. Our results confirmed a dose-dependent infection rate of Ae. albopictus by CHIKV, regardless of the dpe as seen for other arboviruses. Beyond viral oral infectious dose, CHIKV intra-vector dynamics was explosive due to an absence of dissemination barrier, 100% of the mosquitoes exhibiting a disseminated infection regardless of the dose. Furthermore, quantification of transmission rate revealed a time-, dose-dependent but overall weak transmission barrier with individuals transmitting as soon as 2 dpe and >50% of infectious mosquitoes at 6 dpe for the highest dose. Unexpectedly, a higher CHIKV load was found in the saliva of mosquitoes exposed to a high virus dose in the blood meal suggesting a positive correlation between the dose of exposure and the dose delivered by the vector. Based on intra-vector dynamics, epidemiological simulations were conducted using an Agent-Based Model. Even at low mosquito biting rates, CHIKV led to explosive outbreaks suggesting a high epidemic potential of CHIKV with this French metropolitan population of Aedes albopictus.