Polarization-Based Navigation in Drosophila

Abstract

Insects maintain a constant bearing across a wide range of spatial scales. Monarch butterflies and locusts traverse continents (Williams, 1957; Wehner, 1984), and foraging bees and ants travel hundreds of meters to return to their nests (Dyer, 1996; Wehner, 1984, 2003), whereas many other insects fly straight for only a few centimeters before changing direction. Despite this variation in spatial scale, the brain region thought to underlie long-distance navigation is remarkably conserved (Loesel et al., 2002; Homberg, 2008), suggesting that the use of a celestial compass is a general and perhaps ancient capability of insects. Laboratory studies of Drosophila have identified a local search mode in which short, straight segments are interspersed with rapid turns (Mayer et al., 1988; Bender and Dickinson, 2006). However, this flight mode is inconsistent with measured gene flow between geographically separated populations (Jones et al., 1981; Slatkin, 1985; Turelli and Hoffmann, 1991), and individual Drosophila can travel 10 km in a single night (Yerington, 1961; Jones et al., 1981; Coyne et al., 1982, 1987) -- a feat that would be impossible without prolonged periods of straight flight. One well-known cue relevant to orientation and navigation is the pattern of polarization of skylight. To study possible mechanisms of orientation to skylight polarization, we built an arena in which we could observe individual flight responses to rotating the angle of polarized light in the laboratory. We found that flies robustly steer in response to changes in the polarization angle of light. Individual flies also stabilize a particular polarization plane when they are given closed-loop control of such a stimulus. To directly examine orientation behavior under outdoor conditions, we built two portable flight arenas in which a fly viewed the natural sky through a clear aperture. In the first we examined the ability of flies to compensate for external rotations with or without the aid of skylight polarization. The second arena contained a liquid crystal device that could experimentally rotate the polarization angle of the skylight. In both outdoor arenas we tracked fly orientation using a digital video camera and custom computer vision system. Our findings indicate that Drosophila actively orient using the sky's natural polarization pattern.