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Published December 1, 2007 | Published
Journal Article Open

The role of visual and mechanosensory cues in structuring forward flight in Drosophila melanogaster

Abstract

It has long been known that many flying insects use visual cues to orient with respect to the wind and to control their groundspeed in the face of varying wind conditions. Much less explored has been the role of mechanosensory cues in orienting insects relative to the ambient air. Here we show that Drosophila melanogaster, magnetically tethered so as to be able to rotate about their yaw axis, are able to detect and orient into a wind, as would be experienced during forward flight. Further, this behavior is velocity dependent and is likely subserved, at least in part, by the Johnston's organs, chordotonal organs in the antennae also involved in near-field sound detection. These wind-mediated responses may help to explain how flies are able to fly forward despite visual responses that might otherwise inhibit this behavior. Expanding visual stimuli, such as are encountered during forward flight, are the most potent aversive visual cues known for D. melanogaster flying in a tethered paradigm. Accordingly, tethered flies strongly orient towards a focus of contraction, a problematic situation for any animal attempting to fly forward. We show in this study that wind stimuli, transduced via mechanosensory means, can compensate for the aversion to visual expansion and thus may help to explain how these animals are indeed able to maintain forward flight.

Additional Information

© The Company of Biologists Ltd 2007. Accepted 6 August 2007. First published online November 19, 2007. We thank John Bender and Mark Frye for assistance with the magnetic tether apparatus and Andrew Straw for his design of the fly visualization system. We also thank William Dickson for useful discussion and Don Lifke for suggestions on statistical analysis. Finally, we are deeply indebted to Titus Neumann for his assistance with German language translation. This work was supported by award N00014-01-1-0676 from the Office of Naval Research, DAAD19-03-D-0004 from the US Army Research Office, and award DEB-0623527 from the National Science Foundation.

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