1. Department of Bioengineering, California Institute of Technology, Pasadena, California 91125, USA
2. BioCAT and CSRRI, Department BCPS, Illinois Institute of Technology, Chicago, Illinois 60616, USA
3. Department of Molecular Physiology and Biophysics, University of Vermont, Burlington, Vermont 05405, USA
4. Present addresses: Department of Physiology and Biophysics, University of Illinois at Chicago, Chicago, Illinois 60612, USA (G.F.); Department of Physiological Science, University of California, Los Angeles, Los Angeles, California 90095, USA (M.F.).

Correspondence to: Thomas Irving² Correspondence and requests for materials should be addressed to T.I. (Email: irving@iit.edu).

Abstract

Flight in insects—which constitute the largest group of species in the animal kingdom—is powered by specialized muscles located within the thorax. In most insects each contraction is triggered not by a motor neuron spike but by mechanical stretch imposed by antagonistic muscles¹. Whereas 'stretch activation' and its reciprocal phenomenon 'shortening deactivation' are observed to varying extents in all striated muscles, both are particularly prominent in the indirect flight muscles of insects¹. Here we show changes in thick-filament structure and actin–myosin interactions in living, flying Drosophila with the use of synchrotron small-angle X-ray diffraction. To elicit stable flight behaviour and permit the capture of images at specific phases within the 5-ms wingbeat cycle, we tethered flies within a visual flight simulator². We recorded images of 340 s duration every 625 s to create an eight-frame diffraction movie, with each frame reflecting the instantaneous structure of the contractile apparatus. These time-resolved measurements of molecular-level structure provide new insight into the unique ability of insect flight muscle to generate elevated power at high frequency.

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