Computational and experimental insights into the chemosensory navigation of Aedes aegyptimosquito larvae

Abstract

Mosquitoes are prolific disease vectors that affect public health around the world. Although many studies have investigated search strategies used by host-seeking adult mosquitoes, little is known about larval search behaviour. Larval behaviour affects adult body size and fecundity, and thus the capacity of individual mosquitoes to find hosts and transmit disease. Understanding vector survival at all life stages is crucial for improving disease control. In this study, we use experimental and computational methods to investigate the chemical ecology and search behaviour of Aedes aegypti mosquito larvae. We first show that larvae do not respond to several olfactory cues used by adult Ae. aegypti to assess larval habitat quality, but perceive microbial RNA as a potent foraging attractant. Second, we demonstrate that Ae. aegypti larvae use chemokinesis, an unusual search strategy, to navigate chemical gradients. Finally, we use computational modelling to demonstrate that larvae respond to starvation pressure by optimizing exploration behaviour—possibly critical for exploiting limited larval habitat types. Our results identify key characteristics of foraging behaviour in an important disease vector mosquito. In addition to implications for better understanding and control of disease vectors, this work establishes mosquito larvae as a tractable model for chemosensory behaviour and navigation.

Distinct navigation behaviors in Aedes, Anopheles, and Culex mosquito larvae

“…Two stimuli were used: an attractive food solution and quinine, a compound that elicits aversion in Ae. aegypti larvae (Lutz et al, 2019). The food extract solution was made fresh daily by dissolving 0.5% food (Petco; Hikari Tropic First Bites) in Milli-Q water for 1 h, then passing the mixture through a 0.2 μm filter (VWR International, 28145-477) to remove solid particulates.…”

“…We computed the trajectories of individual larvae in a custom behavior arena as previously described (Lutz et al, 2019;Bui et al, 2019). Briefly, individual larvae were introduced to an 8×3 cm rectangular behavior arena containing 20 ml of distilled Milli-Q water.…”

“…1C), and larval behavior was recorded for an additional 15 min. In a separate experiment without larvae, we pipetted 100 µl of fluorescein dye into an identically shaped arena, in order to map stimulus concentration within the arena throughout the 15 min experiment (Lutz et al, 2019) (Fig. 1C).…”

“…1C). Trajectory paths were extracted from each video using Multitracker software by van Breugel et al (2018) and additional code developed previously (Lutz et al, 2019). We visually inspected each trajectory path and manually corrected errors and omissions introduced by the tracking software.…”

“…A previous study has shown that Aedes aegypti larvae find food randomly, rather than demonstrating directed motion toward preferred cues. Once a food-rich area is located, larvae decrease their swimming speed to remain in the favorable environment (Lutz et al, 2019). Previous studies in Anopheles albimanus (Aly and Mulla, 1986) and Aedes vexans (Aly, 1985) larvae showed that these species also discover food at random, although the methods used in these studies prevented deeper analysis into the mechanism of navigation.…”