Wings and halteres act as coupled dual-oscillators in flies

  1. Tanvi Deora
  2. Siddharth S Sane
  3. Sanjay P Sane  Is a corresponding author
  1. Tata Institute of Fundamental Research, India
  2. Azim Premji University, India

Abstract

The mechanics of Dipteran thorax is dictated by a network of exoskeletal linkages which, when deformed by the flight muscles, generate coordinated wing movements. In Diptera, the forewings power flight, whereas the hindwings have evolved into specialized structures called halteres which provide rapid mechanosensory feedback for flight stabilization. Although actuated by independent muscles, wing and haltere motion is precisely phase-coordinated at high frequencies. Because wingbeat frequency is a product of wing-thorax resonance, any wear-and-tear of wings or thorax should impair flight ability. How robust is the Dipteran flight system against such perturbations? Here, we show that wings and halteres are independently-driven, coupled oscillators. We systematically reduced the wing length in flies and observed how wing-haltere synchronization was affected. The wing-wing system is a strongly-coupled oscillator, whereas the wing-haltere system is weakly-coupled through mechanical linkages which synchronize phase and frequency. Wing-haltere link acts in a unidirectional manner; altering wingbeat frequency affects haltere frequency, but not vice-versa. Exoskeletal linkages are thus key morphological features of the Dipteran thorax which ensure wing-haltere synchrony, despite severe wing damage.

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Author details

  1. Tanvi Deora

    National Centre for Biological Sciences, Tata Institute of Fundamental Research, Bangalore, India
    Competing interests
    The authors declare that no competing interests exist.
  2. Siddharth S Sane

    Azim Premji University, Bangalore, India
    Competing interests
    The authors declare that no competing interests exist.
  3. Sanjay P Sane

    Neurobiology, Tata Institute of Fundamental Research, Bangalore, India
    For correspondence
    sane@ncbs.res.in
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8274-1181

Funding

Air Force Office of Scientific Research (FA2386-11-1-4057 and FA9550-16-1-0155)

  • Sanjay P Sane

Human Frontier Science Program

  • Tanvi Deora

National Centre for Biological Sciences

  • Sanjay P Sane

Ramanujan Fellowship, Department of Science and Technology, Government of India

  • Sanjay P Sane

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Gordon J Berman, Emory University, United States

Version history

  1. Received: March 8, 2020
  2. Accepted: November 10, 2021
  3. Accepted Manuscript published: November 16, 2021 (version 1)
  4. Version of Record published: November 26, 2021 (version 2)

Copyright

© 2021, Deora et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Tanvi Deora
  2. Siddharth S Sane
  3. Sanjay P Sane
(2021)
Wings and halteres act as coupled dual-oscillators in flies
eLife 10:e53824.
https://doi.org/10.7554/eLife.53824

Share this article

https://doi.org/10.7554/eLife.53824

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