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Behavioral Flexibility in Drosophila Phototaxis

Animals exhibit innate preferences for different stimulus modalities and intensities, which likely reflect evolutionary responses to specific ecological needs. Insects such as Drosophila move towards a light source when startled. Given the robustness of this response, positive phototaxis has been categorized as an example of hard-wired input-output behaviors. However, classic experiments performed by McEwen in 1918 and Benzer in 1967 demonstrated that wing defects, caused by mutation or damage, profoundly affect phototaxis preferences in walking Drosophila ^1,2. The fact that manipulating an unrelated organ (wings), affects positive phototaxis stands against the hard-wired conception of this behavior, showing that it contains a certain element of flexibility. We hypothesize that phototaxis is not just an automated response, but that there may be a central decision-making stage influenced by a number of environmental and physiological variables, such as flying ability, that are continually monitored. To test our hypothesis we evaluated flies in two different phototactic paradigms (Benzer Countercurrent Apparatus and T-Maze) after altering their flying ability using a range of mechanical and genetic manipulations.

Here we show that flies unable to fly exhibit a negative phototactic behavior. This reversal is not learned, as neither learning mutants nor transgenic flies deficient in various learning paradigms show any deficit, and the effect is immediate. The effect is neither due to injury, as injuries not affecting flight ability do not affect phototaxis. Genetic manipulations preventing the flies from flying but leaving wing-morphology intact also affect phototaxis. Finally, if flying ability is temporarily compromised and then restored, the phototactic behavior changes concomitantly, demonstrating the reversibility of the phototactic effect. These results reveal the flexibility of this taxis, and the existence of an evaluation step prior to behavioral performance.

1. McEwen, R. S. The reactions to light and to gravity in Drosophila and its mutants. J. Exptl. Zool. 25, 49–106 (1918).
2. Benzer, S. BEHAVIORAL MUTANTS OF Drosophila ISOLATED BY COUNTERCURRENT DISTRIBUTION. Proc. Natl. Acad. Sci. U. S. A. 58, 1112–9 (1967).