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bioRxiv · 10.1101/2024.08.31.610631

The complex swarming dynamics of malaria mosquitoes emerges from simple minimally-interactive behavioral rules

Abstract

Swarming is a widespread collective behavior in animals, often thought to emerge from complex interactions among individuals. Here, we show that mating swarms of malaria mosquitoes can emerge from simple behavioral rules with minimal interaction between individuals. We analyzed two published experimental datasets with three-dimensional flight tracks of Anopheles coluzzii mosquitoes swarming above a visual marker under simulated sunset conditions. We found that individuals alternate between straight flight and rapid turning maneuvers known as saccades. These saccades are triggered at the edge of the swarm, and their directions are biased along the sunset direction. This behavior was found consistent between both datasets and across swarm sizes, including solitary individuals, indicating that inter-individual interactions play a limited role within the studied size range. We developed a simple agent-based model incorporating three behavioral rules: attraction to the swarm center, alignment normal to the sunset horizon, both driven by environmental cues, and repulsion through short-range collision avoidance. The model reproduced key features of natural mosquito swarms, including looping flight paths, central density peaks, and directional alignment. Even in the absence of direct inter-individual interactions, the model generated realistic emergent swarm dynamics, demonstrating that social coordination is not required for swarm emergence. Our findings suggest that mosquito swarming is primarily guided by environmental perception rather than social interaction. This minimal framework offers a new perspective on insect swarming and may apply broadly to the many other insect species that form mating swarms. Understanding these rules could inform strategies for vector control and improve the effectiveness of interventions targeting mosquito reproduction. Author SummaryMosquito swarms are a familiar sight in many parts of the world, but the rules that govern their movement have remained mysterious. In our study, we investigated how male malaria mosquitoes behave in mating swarms. Using high-speed videography and computer simulations, we discovered that these swarms do not rely on complex social interactions. Instead, each mosquito follows a few simple rules based on visual cues from the environment, like the position of the sunset and a ground marker. These rules are enough to produce the looping flight patterns and dense swarms observed in nature. Surprisingly, even a single mosquito can perform this behavior in isolation. This minimal approach challenges the idea that swarming requires strong social coordination. It also opens new possibilities for controlling malaria mosquito populations by targeting the environmental factors that influence mating behavior. Since many insects rely on swarming to reproduce, our findings may help explain similar behaviors across species and inform broader strategies for insect population management.

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BibTeXRIS

Cribellier, A., Poda, S., Diabate, A., Roux, O., Muijres, F. T.. 2024-09-02. The complex swarming dynamics of malaria mosquitoes emerges from simple minimally-interactive behavioral rules. https://doi.org/10.1101/2024.08.31.610631

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