Abstract
Mosquitoes infected with malaria parasites have demonstrated altered behaviour that may increase the probability of parasite transmission. Here, we examine the responses of the olfactory system in Plasmodium falciparum infected Anopheles gambiae, Plasmodium berghei infected Anopheles stephensi, and P. berghei infected An. gambiae. Infected and uninfected mosquitoes showed differential responses to compounds in human odour using electroantennography coupled with gas chromatography (GC-EAG), with 16 peaks triggering responses only in malaria-infected mosquitoes (at oocyst, sporozoite or both stages). A selection of key compounds were examined with EAG, and responses showed differences in the detection thresholds of infected and uninfected mosquitoes to compounds including lactic acid, tetradecanoic acid and benzothiazole, suggesting that the changes in sensitivity may be the reason for differential attraction and biting at the oocyst and sporozoite stages. Importantly, the different cross-species comparisons showed varying sensitivities to compounds, with P. falciparum infected An. gambiae differing from P. berghei infected An. stephensi, and P. berghei infected An. gambiae more similar to the P. berghei infected An. stephensi. These differences in sensitivity may reflect long-standing evolutionary relationships between specific Plasmodium and Anopheles species combinations. This highlights the importance of examining different species interactions in depth to fully understand the impact of malaria infection on mosquito olfactory behaviour.
Highlights
The malaria parasite, Plasmodium, alters behavioural responses of Anopheles mosquitoes, the degree of effect and the underlying mechanisms are yet to be fully elucidated[1,2,3,4]
The mechanisms behind the changes in behaviour of infected mosquitoes remain under investigation, with studies in Anopheles stephensi revealing that the same behavioural changes can be instigated through general immune compromise with the bacterium Escherichia coli[1] and suggesting the behaviour may be related to insulin signalling changes taking place upon blood ingestion[32]
A laboratory study by Smallegange et al showed, for the first time in the important malaria vector, Anopheles gambiae, that mosquitoes infected with the transmissible, sporozoite stage of P. falciparum displayed increased behavioural attraction to human volatiles[8], and a study by Cator et al demonstrated increased attraction to human odours in a windtunnel by An. stephensi infected with Plasmodium yoelii[1]
Summary
The malaria parasite, Plasmodium, alters behavioural responses of Anopheles mosquitoes, the degree of effect and the underlying mechanisms are yet to be fully elucidated[1,2,3,4]. A laboratory study by Smallegange et al showed, for the first time in the important malaria vector, Anopheles gambiae, that mosquitoes infected with the transmissible, sporozoite stage of P. falciparum displayed increased behavioural attraction to human volatiles[8], and a study by Cator et al demonstrated increased attraction to human odours in a windtunnel by An. stephensi infected with Plasmodium yoelii[1] These behavioural data suggest that increased behavioural responses to host odour could be mediated through changes in the olfactory system, a hypothesis supported by the latter study’s results that the maxilliary palps exhibited infection-stage dependent differential responses to 1-octen-3-ol, butanoic acid and lactic acid[1]. Cross infections of An. gambiae with P. berghei, which it does not naturally transmit, were conducted to determine whether there is mosquito-parasite species-specificity
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