Oviposition status and sugar availability influence measures of transmission potential in malaria-infected mosquitoes

Abstract

ABSTRACTBackgroundLike other oviparous organisms, the gonotrophic cycle of mosquitoes is not complete until they have selected a suitable habitat to oviposit. In addition to the evolutionary constraints associated with selective oviposition behavior, the physiological demands relative to an organism’s oviposition status also influences their nutrient requirement from the environment. Yet, studies that measure transmission potential (vectorial capacity or competence) of mosquito-borne parasites rarely consider if the rates of parasite replication and development could be influenced by these constraints resulting from whether mosquitoes have completed their gonotrophic cycle.MethodsAnopheles stephensimosquitoes were infected withPlasmodium bergheithe rodent analog of human malaria and maintained on 1% or 10% dextrose and either provided oviposition sites (‘oviposited’ herein) to complete their gonotrophic cycle or forced to retain eggs (‘non-oviposited’). Transmission potential in the four groups was measured up to 27 days post-infection as 1) the rates of vector survival, 2) rates of sporozoite migration to the salivary glands (‘extrinsic incubation period’ or EIP), and 3), sporozoite densities.ResultsIn the two groups of oviposited mosquitoes, rates of sporozoite migration and densities in the salivary glands were clearly higher in mosquitoes fed 10% dextrose. In non-oviposited mosquitoes however, rates of sporozoite migration and densities were independent of sugar concentrations, although both measures were slightly lower than oviposited mosquitoes fed 10% dextrose. Rates of vector survival were higher in non-oviposited mosquitoes.ConclusionsTaken together, these results suggest vectorial capacity for malaria parasites may be dependent on nutrient availability and oviposition/gonotrophic status and as such, argue for more careful consideration of this interaction when estimating transmission potential; costs to parasite fitness and vector survival were buffered against changes in nutritional availability from the environment in non-oviposited mosquitoes, but not oviposited mosquitoes. In general, however, these patterns suggest parasite fitness may be dependent on complex interactions between physiological (nutrition) and evolutionary (egg-retention) trade-offs in the vector, with potential implications for disease transmission and management. For instance, while reducing availability of oviposition sites and environmental sources of nutrition are key components of integrated vector management strategies, their abundance and distribution is under strong selection pressure from the patterns associated with climate change.Graphical abstract