Flying Drosophila Orient to Sky Polarization

Abstract

Summary Insects maintain a constant bearing across a wide range of spatial scales. Monarch butterflies and locusts traverse continents [1, 2], foraging bees and ants travel hundreds of meters to return to their nest [1, 3, 4], 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 [5, 6], suggesting that the use of celestial cues for navigation is a general and perhaps ancient behavioral capability of insects. Laboratory studies of Drosophila have identified a local search mode in which short straight segments are interspersed with rapid turns [7, 8]. Such flight modes, however, are inconsistent with measures of gene flow between geographically-separated populations [9-11], and individual Drosophila have been observed to travel 10 km across desert terrain in a single night [9, 12, 13] – a feat that would be impossible without prolonged periods of straight flight. To directly examine orientation behavior under outdoor conditions, we built a portable flight arena in which a fly viewed the natural sky through a liquid crystal device that could experimentally rotate the angle of polarization. Our findings indicate that flying Drosophila actively orient using the sky's natural polarization pattern.

Opsin expression, physiological characterization and identification of photoreceptor cells in the dorsal rim area and main retina of the desert locust,Schistocerca gregaria

“…Polarotactic orientation has been demonstrated in field experiments in the desert ant (Wehner and Müller, 2006), the honeybee (von Frisch, 1949), several species of dung beetles (Dacke et al, 2003;Dacke et al, 2011), the monarch butterfly (Reppert et al, 2004) and the fruitfly (Weir and Dickinson, 2012) and, in laboratory experiments, in the house fly (von Philipsborn and Labhart, 1990), the field cricket (Brunner and Labhart, 1987), and the desert locust (Mappes and Homberg, 2004). In all of these insects, POL detection is mediated by a small dorsal rim area (DRA) in the compound eye (Labhart and Meyer, 1999).…”

Diurnal dung beetles use the intensity gradient and the polarization pattern of the sky for orientation

“…In 1949, von Frisch was the first to describe the use of polarized skylight for orientation in honey bees (von Frisch, 1949). Since then, compass orientation based on the skylight polarization pattern has been shown in several diurnal insects, including desert ants, monarch butterflies and fruit flies (Wehner, 1997;Reppert et al, 2004;Weir and Dickinson, 2012). In all these species, a relatively small region of the eye -the dorsal rim area -is specialized for polarization vision (Labhart and Meyer, 1999); painting out this area leads to a loss of perception of polarized skylight (Wehner, 1989).…”

High e-vector acuity in the polarisation vision system of the fiddler crabUca vomeris

“…Animals, however, are known to use polarised light for a range of tasks, including the detection of bodies of water by airborne insects using surface-reflected polarised light (Schwind, 1983;Schwind, 1991;Kriska et al, 1998;Horváth et al, 2011), intra-specific communication with inbuilt polarised body patterns Chiou et al, 2008;Chiou et al, 2011), and navigation and orientation using the pattern of celestial polarised light (von Frisch, 1949;Wehner, 1976;Dacke et al, 2003;Weir and Dickinson, 2012). Some animals, such as cephalopods, have apparently evolved an acute polarisation sense as a substitute for colour vision (Moody and Parriss, 1961;Messenger, 1981;Marshall et al, 1999;Temple et al, 2012).…”