Plasmodium parasites manipulate mosquitoes' olfaction behavior to increase their malaria transmission potential

The epidemiological success of an insect-vector-borne disease may be influenced by the pathogen’s ability to modify its insect host’s behavior. Malaria parasites in the genus Plasmodium have been shown to be able to alter various aspects of their mosquito vector’s biting behavior in ways that could increase their transmission success (Koella 1999). During host seeking, mosquitoes respond to visual cues, heat, and volatile chemical emissions such as carbon dioxide, lactic acid and fatty acids that are typical of vertebrate hosts (Allan et al. 1987, Sutcliffe 1987). We measured the olfactory neuronal responses of blood-fed versus sugar-water-fed Anopheles stephensi female mosquitoes using electropalpogram (EPG) recordings to different odorants at different times following female blood-feeding. EPG amplitudes differed significantly according to days post-blood-feeding and also differed from sugar-water-fed control group females. Further recordings using females infected with the rodent malaria parasite, Plasmodium yoelii, showed that P. yoelii infection caused female An. stephensi EPGs to differ significantly from those recorded from blood-fed but uninfected females. EPG responses to a variety of volatile odorants were monitored over Days 0, 1, 4, 7, 8, 10, 11, 14, 15, 18, 21, 24 and 29 post-blood-meal. The recordings showed that the responses of peripheral olfactory receptor neurons are correlated with the different stages of P. yoelii development within the mosquito. Infected mosquitoes showed significantly lower amplitude EPG responses during the oocyst (non-transmissible) stage of malaria infection, and significantly higher EPGs during the sporozoite (transmissible) stage of infection. These results show that P. yoelii can alter olfactory receptor neuron response sensitivity and suggests that this might influence the host-seeking behavior of An. stephensi females in a way that would improve the transmission of this species of malaria parasite. This is the first study that reports such alterations of mosquito peripheral olfactory neuron responses by a Plasmodium parasite. Such olfactory modulation of response to odorants during different stages of Plasmodium infection could possibly play a significant role in the parasite transmission process. Understanding how such shifts in receptor neuron sensitivity might influence host-odor-mediated behavior may contribute to the development of new control and monitoring/detection strategies that can utilize these behaviors against disease vectors.