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How mosquitoes determine which individuals to bite has important epidemiological consequences. This choice is not random; most mosquitoes specialize in one or a few vertebrate host species, and some individuals in a host population are preferred over others. Mosquitoes will also blood feed from other hosts when their preferred is no longer abundant, but the mechanisms mediating these shifts between hosts, and preferences for certain individuals within a host species, remain unclear. Here, we show that olfactory learning may contribute to Aedes aegypti mosquito biting preferences and host shifts. Training and testing to scents of humans and other host species showed that mosquitoes can aversively learn the scent of specific humans and single odorants and learn to avoid the scent of rats (but not chickens). Using pharmacological interventions, RNAi, and CRISPR gene editing, we found that modification of the dopamine-1 receptor suppressed their learning abilities. We further show through combined electrophysiological and behavioral recordings from tethered flying mosquitoes that these odors evoke changes in both behavior and antennal lobe (AL) neuronal responses and that dopamine strongly modulates odor-evoked responses in AL neurons. Not only do these results provide direct experimental evidence that olfactory learning in mosquitoes canplay an epidemiological role, but collectively, they also provide neuroanatomical and functional demonstration of the role of dopamine in mediating this learning-induced plasticity, for the first time in a disease vector insect.

Animals face the daunting task of controlling their limbs using a small set of highly constrained actuators. This problem is particularly demanding for insects such as Drosophila, which must adjust wing motion for both quick voluntary maneuvers and slow compensatory reflexes using only a dozen pairs of muscles. To identify strategies by which animals execute precise actions using sparse motor networks, we imaged the activity of a complete ensemble of wing control muscles in intact, flying flies. Our experiments uncovered a remarkably efficient logic in which each of the four skeletal elements at the base of the wing are equipped with both large phasically active muscles capable of executing large changes and smaller tonically active muscles specialized for continuous fine-scaled adjustments. Based on the responses to a broad panel of visual motion stimuli, we have developed a model by which the motor array regulates aerodynamically functional features of wing motion. VIDEO ABSTRACT.

SummaryAn important role of visual systems is to detect nearby predators, prey, and potential mates [1], which may be distinguished in part by their motion. When an animal is at rest, an object moving in any direction may easily be detected by motion-sensitive visual circuits [2, 3]. During locomotion, however, this strategy is compromised because the observer must detect a moving object within the pattern of optic flow created by its own motion through the stationary background. However, objects that move creating back-to-front (regressive) motion may be unambiguously distinguished from stationary objects because forward locomotion creates only front-to-back (progressive) optic flow. Thus, moving animals should exhibit an enhanced sensitivity to regressively moving objects. We explicitly tested this hypothesis by constructing a simple fly-sized robot that was programmed to interact with a real fly. Our measurements indicate that whereas walking female flies freeze in response to a regressively moving object, they ignore a progressively moving one. Regressive motion salience also explains observations of behaviors exhibited by pairs of walking flies. Because the assumptions underlying the regressive motion salience hypothesis are general, we suspect that the behavior we have observed in Drosophila may be widespread among eyed, motile organisms.

Unlike creatures that walk, flying animals need to control their horizontal motion as well as their height above the ground. Research on insects, the first animals to evolve flight, has revealed several visual reflexes that are used to govern horizontal course. For example, insects orient toward prominent vertical features in their environment [1], [2], [3], [4] and [5] and generate compensatory reactions to both rotations [6] and [7] and translations [1], [8], [9], [10] and [11] of the visual world. Insects also avoid impending collisions by veering away from visual expansion [9], [12], [13] and [14]. In contrast to this extensive understanding of the visual reflexes that regulate horizontal course, the sensory-motor mechanisms that animals use to control altitude are poorly understood. Using a 3D virtual reality environment, we found that Drosophila utilize three reflexes—edge tracking, wide-field stabilization, and expansion avoidance—to control altitude. By implementing a dynamic visual clamp, we found that flies do not regulate altitude by maintaining a fixed value of optic flow beneath them, as suggested by a recent model [15]. The results identify a means by which insects determine their absolute height above the ground and uncover a remarkable correspondence between the sensory-motor algorithms used to regulate motion in the horizontal and vertical domains.