Environmental influence on the genetic basis of mosquito resistance to malaria parasites

Abstract

The genetic basis of a host's resistance to parasites has important epidemiological and evolutionary consequences. Understanding this genetic basis can be complicated by non-genetic factors, such as environmental quality, which may influence the expression of genetic resistance and profoundly alter patterns of disease and the host's response to selection. In particular, understanding the environmental influence on the genetic resistance of mosquitoes to malaria gives valuable knowledge concerning the use of malaria-resistant transgenic mosquitoes as a measure of malaria control. We made a step towards this understanding by challenging eight isofemale lines of the malaria vector Anopheles stephensi with the rodent malaria parasite Plasmodium yoelii yoelii and by feeding the mosquitoes with different concentrations of glucose. The isofemale lines differed in infection loads (the numbers of oocysts), corroborating earlier studies showing a genetic basis of resistance. In contrast, the proportion of infected mosquitoes did not differ among lines, suggesting that the genetic component underlying infection load differs from the genetic component underlying infection rate. In addition, the mean infection load and, in particular, its heritable variation in mosquitoes depended on the concentration of glucose, which suggests that the environment affects the expression and the evolution of the mosquitoes' resistance in nature. We found no evidence of genotype-by-environment interactions, i.e. the lines responded similarly to environmental variation. Overall, these results indicate that environmental variation can significantly reduce the importance of genes in determining the resistance of mosquitoes to malaria infection.

Figure 1

Genetic and environmental components of infection load. The mean numbers of oocysts in infected mosquitoes and their standard errors are given for eight isofemale lines fed on 2% (white bars), 4% (grey bars) and 6% (black bars) glucose solutions. The lines are ranked along the x-axis according to their mean number of oocysts (averaged across glucose concentrations). The numbers of oocysts have been transformed using the square root and corrected for the mice used to feed the mosquitoes (the residual gives the difference to the average for a given mouse).

Figure 2

Genetic and environmental components of parasite-induced mortality. Mortality that occurred during 8 days following an infected or an uninfected blood meal is given for mosquitoes fed on (a) 2%, (b) 4% and (c) 6% glucose solutions in eight isofemale lines. Each pair of connected symbols represents a different mosquito line.