Wings and halteres act as coupled dual-oscillators in flies

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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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The following data sets were generated

1. Deora T
2. Sane S
(2020) The coupled dual-oscillator model of wing and haltere motion in flies
Dryad Digital Repository, doi:10.5061/dryad.hqbzkh1cc.

https://doi.org/10.5061/dryad.hqbzkh1cc

Article and author information

Author details

Tanvi Deora

National Centre for Biological Sciences, Tata Institute of Fundamental Research, Bangalore, India

Competing interests
The authors declare that no competing interests exist.
Siddharth S Sane

Azim Premji University, Bangalore, India

Competing interests
The authors declare that no competing interests exist.
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.

"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.

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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.