A persistent behavioral state enables sustained predation of humans by mosquitoes

SUMMARY

Predatory animals first detect, then pursue, and ultimately capture prey. Sensory cues, including scent emitted by prey, are detected by the predator and used to guide pursuit. Because the pursuit phase can last for extended periods of time, it is critical for predators to persist in the chase even when prey is difficult to detect in a noisy sensory landscape. It is equally important for predators to abandon pursuit if enough time has elapsed that prey capture is unlikely to occur. We studied prey detection and sustained pursuit in the mosquito Aedes aegypti, a micropredator of humans. These animals first detect humans through sensory cues that are emitted at a distance such as carbon dioxide in breath and odor from skin. As the mosquito approaches a human, additional cues such as body heat and visual contrast signal the promise of a blood meal, which females need to produce eggs. To study how initial prey detection influences the duration of pursuit, we developed optogenetic tools to induce a brief fictive sensation of carbon dioxide and used machine learning-based classification of behavior to investigate how mosquitoes respond to subsequent human cues. We found that a 5-second optogenetic pulse of fictive carbon dioxide induced a persistent behavioral state in female mosquitoes that lasted for more than 10 minutes. This state is highly specific to females searching for a blood meal and was not induced in recently blood-fed females or in males, who do not feed on blood. In males that lack the gene fruitless, which controls persistent social behaviors in other insects, fictive carbon dioxide induced a long-lasting behavior response resembling the predatory state of females. Finally, we show that the persistent state triggered by detection of fictive carbon dioxide enabled females to engorge on a blood meal mimic offered up to 14 minutes after the initial stimulus. Our results demonstrate that a persistent internal state allows female mosquitoes to integrate multiple human sensory cues over long timescales, an ability that is key to their success as an apex micropredator of humans.