Filarial infection influences mosquito behaviour and fecundity

Abstract

Understanding vector-parasite interactions is increasingly important as we move towards the endpoint goals set by the Global Programme for the Elimination of Lymphatic Filariasis (GPELF), as interaction dynamics may change with reduced transmission pressure. Elimination models used to predict programmatic endpoints include parameters for vector-specific transmission dynamics, despite the fact that our knowledge of the host-seeking behaviour of filariasis infected mosquitoes is lacking. We observed a dynamic, stage-specific and density dependent change in Aedes aegypti behaviour towards host cues when exposed to Brugia malayi filarial parasites. Infected mosquitoes exhibited reduced activation and flight towards a host during the period of larval development (L1/L2), transitioning to a 5 fold increase in activation and flight towards a host when infective stage larvae (L3) were present (p < 0.001). In uninfected control mosquitoes, we observed a reduction in convergence towards a host during the same period. Furthermore, this behaviour was density dependent with non-activated mosquitoes harbouring a greater burden of L1 and L2 larvae while activated mosquitoes harboured a greater number of L3 (p < 0.001). Reductions in fecundity were also density-dependent, and extended to mosquitoes that were exposed to microfilariae but did not support larval development.

Figure 1. Incidence rate ratio (IRR) of mosquito convergence in the presence of host cues.

(a) Converging mosquitoes at the developing stage (4–6 DPE) compared to the control cohort. (b) Converging mosquitoes at the infective stage (11–13 DPE) compared to the control cohort. All observed behaviours were significantly different than the control un-infected mosquitoes at both time points (p < 0.0001). Control (n = 790), Low Density (n = 250), High density (n = 930).

Figure 2. Worm burden in mosquitoes that converged on a host and those that remained in the holding cage at developing (4–6 DPE) and infective (11–13 DPE) life stages.

Dark lines show mean worm burden of converging and non-converging mosquitoes.

Figure 3. Mean number of mature eggs, including those laid or mature but free inside the abdomen, in unexposed mosquitoes (n = 20) and B. malayi exposed mosquitoes (n = 52) with 0–5 larvae present.

Only 2 mosquitoes carried 5 larvae and neither of these had developed eggs therefore categories 4 and 5 where combined for statistical analysis. All mosquitoes had mated. Results with the same letter above the bar are not statistically significant from each other.