Variation in tolerance to parasites in natural Asian tiger mosquito populations and its effect on vectorial capacity

Abstract

The vectorial capacity of mosquitoes depends upon the magnitude of reduction of parasite load upon infection through resistance mechanisms (e.g., immune-mediated killing) and the ability of mosquitoes to offset infection-mediated costs through tolerance mechanisms (e.g., tissue repair). Here we use a common-garden experimental framework to measure variation in resistance and tolerance to dog heartworm (Dirofilaria immitis) between natural Aedes albopictus mosquito populations representing areas of low and high transmission intensity. Our data revealed that survival to the extrinsic incubation period, the earliest time point at which infective L3 larvae develop, significantly differed between populations (ranging from 10-60%) when mosquitoes infected with D. immitis at both the low (15 microfilaria/l blood) and high (30 microfilaria/l blood) infection dose (Dose: {chi}2 = 191.473; P < 0.001; Population: {chi}2 = 24.485; P = 0.001; Dose x Population: {chi}2 = 35.566; P = 0.001). Contrary to expectations, we found that mosquito populations with highest resistance (i.e., greatest reduction in parasite load) also exhibited highest mortality upon infection (F1,12 = 6.781, P = 0.023; Dose: F1,12 = 6.747; P = 0.023; Mortality x Dose: F1,12 = 0.111, P = 0.744). Expressing the effect of the number of killed (NKILLED) and live (NLIVE) parasite on survival of mosquitoes from the different population, we document a significant inter-population variation in the survival cost of additional parasite (i.e., tolerance to infection (NLIVE x Population: {chi}2 = 22.845; P = 0.002; NKILLED x Population: {chi}2 = 31.959; P = < 0.001; NLIVE x NKILLED x Population: {chi}2 = 22.266; P = 0.002), in conjunction with negative relationship between tolerance and resistance (Resistance: F1,12 = 11.870, P = 0.005; Dose: F1,12 = 16.0170, P = 0.002; Resistance x Dose: F1,12 = 9.699, P =0.009). Importantly, populations from areas with high transmission intensity (as measured by parasite prevalence in dogs) showed elevated tolerance (Prevalence: F1,12 = 9.5, P = 0.012; Prevalence2: F1,12 = 4.353, P = 0.064; Dose: F1,12 = 38.855, P = <0.001), and these populations were also associated with increased vectorial capacity (Tolerance: F1,12 = 8.175, P = 0.014; Dose: F1,12 = 0.005, P = 0.946; Tolerance x Dose: F1,12 = 0.920, P = 0.356). Consequently, our data indicate that spatial variation in disease transmission intensity is linked to the evolution of tolerance in natural mosquito populations, which in turn can feedback to impact disease risk.