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Molecular dynamics of cyclically contracting insect flight muscle in vivo

Nature volume 433, pages 330–334 (2005)Cite this article

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 µs duration every 625 µs 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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Figure 1: Experimental arrangement.
Figure 2: X-ray patterns from live flies.
Figure 3: Changes in diffraction features as a function of phase of the wingbeat cycle.

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Acknowledgements

We thank J. Costello for help with data analysis, J. Fockler for computer programming, and D. Swank, R. Tregear, M. K. Reedy and M. C. Reedy for helpful discussions. The research was supported by NIH. The APS is supported by the US Department of Energy. BioCAT is a NIH-supported Research Center.

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Author notes

  1. Gerrie Farman

    Present address: Department of Physiology and Biophysics, University of Illinois at Chicago, Chicago, Illinois, 60612, USA

  2. Mark Frye

    Present address: Department of Physiological Science, University of California, Los Angeles, Los Angeles, California, 90095, USA

Authors and Affiliations

  1. Department of Bioengineering, California Institute of Technology, Pasadena, California, 91125, USA

    Michael Dickinson & Mark Frye

  2. BioCAT and CSRRI, Department BCPS, Illinois Institute of Technology, Chicago, Illinois, 60616, USA

    Gerrie Farman, Tanya Bekyarova, David Gore & Thomas Irving

  3. Department of Molecular Physiology and Biophysics, University of Vermont, Burlington, Vermont, 05405, USA

    David Maughan

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  1. Michael Dickinson
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Correspondence to Thomas Irving.

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Supplementary information

Supplementary Video 1

Changes in X-ray diffraction patterns during a wingbeat. Animation consisting of background subtracted X-ray diffraction patterns from live Drosophila metleri at each time point in the wingbeat cycle along with cartoons showing wing position and relative length of the DLMs and DVMs (length changes exaggerated 10-fold). Initially 2 s per frame and then 10 wingbeats/8s (MOV 5893 kb)

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Dickinson, M., Farman, G., Frye, M. et al. Molecular dynamics of cyclically contracting insect flight muscle in vivo. Nature 433, 330–334 (2005). https://doi.org/10.1038/nature03230

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