Variation in Tolerance to Parasites Affects Vectorial Capacity of Natural Asian Tiger Mosquito Populations

Abstract

Globally, diseases transmitted by arthropod vectors, such as mosquitoes, remain a major cause of morbidity and mortality. The defense responses of mosquito and other arthropod vectors against parasites has long been recognized central to understanding disease transmission and for the development of novel disease control strategies. Consequently, the mechanisms by which mosquitoes resist parasitic infection (e.g. immune-mediated killing) have long been studied. However, the ability of mosquitoes to ameliorate the negative fitness consequences of infection through tolerance mechanisms (e.g. tissue repair) has been virtually ignored. Ignoring anti-pathogen tolerance is especially taxing in vector biology because unlike resistance, which typically reduces vectorial capacity, tolerance is expected to increase vectorial capacity by reducing parasite-mediated mortality without killing parasites, contributing to the recurrent emergence of vector-borne diseases, its stabilization, and exacerbation. Despite its importance there is currently no evidence for the evolution of tolerance in natural mosquito populations. Here we use a common-garden experimental framework to measure variation in resistance and tolerance to dog heartworm (Dirofilaria immitis) between eight natural Aedes albopictus mosquito populations representing areas of low and high transmission intensity. We find significant inter-population variation in tolerance and elevated tolerance where transmission intensity is high. Additionally, as expected we find that increased tolerance is associated with higher vectorial capacity. Consequently, our results indicate that high transmission intensity can lead to the evolution of more competent disease vectors, which can feedback to impact disease risk.