Sex-specific effects of an avian malaria parasite on an insect vector: support for the resource limitation hypothesis

Many parasites, such as those that cause malaria, depend on an insect vector for transmission between vertebrate hosts. Theory predicts that parasites should have little or no effect on the transmission ability of vectors, e.g., parasites should not reduce vector life span as this will limit the temporal window of opportunity for transmission. However, if the parasite and vector compete for limited resources, there may be an unavoidable physiological cost to the vector (resource limitation hypothesis). If this cost reduces vector fitness, then the effect should be on reproduction, not survival. Moreover, in cases where both sexes act as vectors, the effect should be greater on females than males because of the greater cost of reproduction for females. We tested these predictions using Haemoproteus columbae, a malaria parasite of Rock Pigeons (Columba livia) that is vectored by both sexes of the hippoboscid fly Pseudolynchia canariensis, Hippoboscids belong to a group of insects (Hippoboscoidea) with unusually high female reproductive investment; eggs hatch in utero, and each larva progresses through three stages, feeding from internal “milk” glands in the female, followed by deposition as a large puparium. We compared fitness components for flies feeding on malaria-infected vs. uninfected Rock Pigeons. Survival of female flies decreased significantly when they fed on infected birds, while survival of male flies was unaffected. Our results were contrary to the overall prediction that malaria parasites should have no effect on vector survival, but consistent with the prediction that an effect, if present, would be greater on females. As predicted, females feeding on malaria-infected birds produced fewer offspring, but there was no effect on the quality of offspring. A separate short-term feeding experiment confirmed that female flies are unable to compensate for resource limitation by altering blood meal size. The unanticipated effect on female survival may be explained by the fact that H. columbae also has the option of using male flies as vectors.