Resource Localization and Multimodal Flight Control in Drosophila melanogaster

Upwind flight is a common strategy among insects searching for the sources of attractive odors. While much is known about the behavior of male Lepidoptera tracking female pheromone plumes, data on odor localization in other taxa, including the model organism Drosophila melanogaster, have been relatively lacking. The work presented in this thesis provides a description of the multimodal control of forward flight in D. melanogaster, including olfactory mediated flight during the localization of attractive resources. Here it is shown that D. melanogaster responds rapidly to the onset of olfactory stimulation by turning upwind and increasing its airspeed, yielding an upwind surge. Following plume loss, flies, like many moths, often cast—flying perpendicular to the wind while making iterated large-angle turns. Flies, however, are anemotactic even in the absence of odor, and unlike many Lepidoptera, they also fly fast and straight upwind in a homogenous odor cloud. Though they respond rapidly to odor contact and loss, flies thus do not require intermittent olfactory stimulation in order to sustain upwind flight. The results of tethered-flight experiments are largely in accord with those from free-flight. Pulsed and continuous olfactory stimuli elicit qualitatively similar responses in the wing kinematics of tethered flies, suggesting that the intermittency of the odor plume is not a key parameter in modulating flight behavior. At the same time, a tethered-flight analogue of casting may preferentially follow exposure to brief odor pulses, suggesting that pulse duration is an important factor in shaping flight trajectories. The role of mechanosensory cues in the orientation of flying insects has been the focus of relatively little research. The results presented here suggest that a strong mechanosensory response orients flying flies into an oncoming wind, as would be experienced during forward flight. This response is mediated by the Johnston’s organs and may play an essential role during forward flight. Expanding visual stimuli, which necessarily accompany forward translation, normally elicit a robust turning response in flies. The wind orientation response described here is sufficient to suppress this visual reflex, however, potentially explaining how flies are able to successfully fly forward while searching for attractive resources.