Biomechanical basis of wing and haltere coordination in flies

Edited by M. A. R. Koehl, University of California, Berkeley, CA, and approved December 16, 2014 (received for review June 30, 2014)
January 20, 2015
112 (5) 1481-1486

Significance

Insect wing movements must be both precise and fast. This requirement is especially challenging in smaller insects whose flapping frequencies exceed 100 Hz, because the nervous system cannot exercise stroke-by-stroke control at such rates. In flies, the hind wings have evolved into halteres, gyroscopic sense organs that oscillate exactly antiphase to wings. We show that wing–wing and wing–haltere coordination at high frequencies is mediated by passive biomechanical linkages in thorax. This system requires a clutch mechanism in the wing hinge to independently engage each wing with the vibrating thorax. Once the wings are engaged, the gearbox modulates the amplitude of each wing. Thus, the force transmission mechanism from thorax to wings in flies bears remarkable similarity to automobile transmission systems.

Abstract

The spectacular success and diversification of insects rests critically on two major evolutionary adaptations. First, the evolution of flight, which enhanced the ability of insects to colonize novel ecological habitats, evade predators, or hunt prey; and second, the miniaturization of their body size, which profoundly influenced all aspects of their biology from development to behavior. However, miniaturization imposes steep demands on the flight system because smaller insects must flap their wings at higher frequencies to generate sufficient aerodynamic forces to stay aloft; it also poses challenges to the sensorimotor system because precise control of wing kinematics and body trajectories requires fast sensory feedback. These tradeoffs are best studied in Dipteran flies in which rapid mechanosensory feedback to wing motor system is provided by halteres, reduced hind wings that evolved into gyroscopic sensors. Halteres oscillate at the same frequency as and precisely antiphase to the wings; they detect body rotations during flight, thus providing feedback that is essential for controlling wing motion during aerial maneuvers. Although tight phase synchrony between halteres and wings is essential for providing proper timing cues, the mechanisms underlying this coordination are not well understood. Here, we identify specific mechanical linkages within the thorax that passively mediate both wing–wing and wing–haltere phase synchronization. We demonstrate that the wing hinge must possess a clutch system that enables flies to independently engage or disengage each wing from the mechanically linked thorax. In concert with a previously described gearbox located within the wing hinge, the clutch system enables independent control of each wing. These biomechanical features are essential for flight control in flies.

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Acknowledgments

We thank Anand Krishnan, Umesh Mohan, and Aparna Nair for assisting the study, and L. Kundanati and N. Gundiah from the Indian Institute of Science, Bangalore, for help with SEM. This study was funded by the Air Force Office of Scientific Research, Asian Office of Aerospace Research and Development (AOARD 114057), International Technology Center–Pacific, and a Ramanujan fellowship from the Department of Science and Technology, Government of India (to S.P.S.).

Supporting Information

Supporting Information (PDF)
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References

1
AA Polilov, The smallest insects evolve anucleate neurons. Arthropod Struct Dev 41, 29–34 (2012).
2
R Dudley The Biomechanics of Insect Flight (Princeton Univ Press, Princeton, NJ, 2000).
3
RK Josephson, JG Malamud, DR Stokes, Asynchronous muscle: A primer. J Exp Biol 203, 2713–2722 (2000).
4
MH Dickinson, MS Tu, The function of dipteran flight muscle. Comp Biochem Physiol A 116, 223–238 (1997).
5
J Bastian, H Esch, Nervous control of indirect flight muscles of honey bee. Z Vgl Physiol 67, 307 (1970).
6
KD Roeder, Movements of the thorax and potential changes in the thoracic muscles of insects during flight. Biol Bull 100, 95–106 (1951).
7
RF Chapman The Insects (Harvard Univ Press, 3rd Ed, Cambridge, MA, 1982).
8
JWS Pringle, The Croonian Lecture, 1977. Stretch activation of muscle: Function and mechanism. Proc R Soc Lond B Biol Sci 201, 107–130 (1978).
9
A Wisser, W Nachtigall, Functional-morphological investigations on the flight muscles and their insertion points in the blowfly Calliphora-erythrocephala (insecta, Diptera). Zoomorphology 104, 188–195 (1984).
10
G Nalbach, The halteres of the blowfly Calliphora.1. Kinematics and dynamics. J Comp Physiol A 173, 293–300 (1993).
11
G Nalbach, Extremely non-orthogonal axes in a sense organ for rotation: Behavioural analysis of the dipteran haltere system. Neuroscience 61, 149–163 (1994).
12
JL Fox, TL Daniel, A neural basis for gyroscopic force measurement in the halteres of Holorusia. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 194, 887–897 (2008).
13
JWS Pringle, The gyroscopic mechanism of the halteres of Diptera. Philos Trans R Soc Lond B Biol Sci 233, 347–384 (1948).
14
A Fayyazuddin, MH Dickinson, Convergent mechanosensory input structures the firing phase of a steering motor neuron in the blowfly, Calliphora. J Neurophysiol 82, 1916–1926 (1999).
15
A Sherman, MH Dickinson, A comparison of visual and haltere-mediated equilibrium reflexes in the fruit fly Drosophila melanogaster. J Exp Biol 206, 295–302 (2003).
16
JM Goldberg, PB Brown, Response of binaural neurons of dog superior olivary complex to dichotic tonal stimuli: Some physiological mechanisms of sound localization. J Neurophysiol 32, 613–636 (1969).
17
EG Boettiger, E Furshpan, The mechanics of flight movements in Diptera. Biol Bull 102, 200–211 (1952).
18
SH Strogatz Non-linear Dynamics and Chaos (Perseus, New York, 1994).
19
W Nachtigall, DM Wilson, Neuro-muscular control of dipteran flight. J Exp Biol 47, 77–97 (1967).
20
HC Bennet-Clark, AW Ewing, The wing mechanism involved in the courtship of Drosophila. J Exp Biol 49, 117–128 (1968).
21
G Nalbach, The gear change mechanism of the blowfly (Calliphora erythrocephala) in tethered flight. J Comp Physiol A 165, 321–331 (1989).
22
A Wisser, Wing beat of Calliphora erythrocephala: Turning axis and gearbox of the wing base (insecta, Diptera). Zoomorphology 107, 359–369 (1988).
23
JA Miyan, AW Ewing, Further observations on Dipteran flight: Details of the mechanism. J Exp Biol 136, 229–241 (1988).
24
JA Miyan, AW Ewing, How Diptera move their wings: A re-examination of the wing base articulation and muscle systems concerned with flight. Philos Trans R Soc London Ser B Biol Sci 311, 271–302 (1985).
25
JA Miyan, AW Ewing, A wing synchronous receptor for the Dipteran flight motor. J Insect Physiol 30, 567–574 (1984).
26
W Nachtigall, A Wisser, D Eisinger, Flight of the honey bee. VIII. Functional elements and mechanics of the “flight motor” and the wing joint—one of the most complicated gear-mechanisms in the animal kingdom. J Comp Physiol B 168, 323–344 (1998).
27
CN Balint, MH Dickinson, The correlation between wing kinematics and steering muscle activity in the blowfly Calliphora vicina. J Exp Biol 204, 4213–4226 (2001).
28
JA Miyan, AW Ewing, Is the click mechanism of Dipteran flight and artifact of CCL4 anesthesia. J Exp Biol 116, 313–322 (1985).
29
AR Ennos, A comparative-study of the flight mechanism of Diptera. J Exp Biol 127, 355–372 (1987).
30
HK Pfau, Critical comments on a ‘novel mechanical model of dipteran flight’. J Exp Biol 128, 463–468 (1987).
31
M Burrows, Energy storage and synchronisation of hind leg movements during jumping in planthopper insects (Hemiptera, Issidae). J Exp Biol 213, 469–478 (2010).
32
D Leston, JWS Pringle, DCS White, Muscular activity during preparation for flight in a beetle. J Exp Biol 42, 409–414 (1965).
33
RJ Wootton Flying Insects and Robots, eds D Floreano, JC Zufferey, MV Srinivasan, C Ellington (Springer, Heidelberg), pp. 207–217 (2010).
34
SN Patek, DM Dudek, MV Rosario, From bouncy legs to poisoned arrows: Elastic movements in invertebrates. J Exp Biol 214, 1973–1980 (2011).

Information & Authors

Information

Published in

Go to Proceedings of the National Academy of Sciences
Proceedings of the National Academy of Sciences
Vol. 112 | No. 5
February 3, 2015
PubMed: 25605915

Classifications

Submission history

Published online: January 20, 2015
Published in issue: February 3, 2015

Keywords

  1. insect thorax
  2. halteres
  3. insect wings
  4. wing hinge
  5. wing clutch

Acknowledgments

We thank Anand Krishnan, Umesh Mohan, and Aparna Nair for assisting the study, and L. Kundanati and N. Gundiah from the Indian Institute of Science, Bangalore, for help with SEM. This study was funded by the Air Force Office of Scientific Research, Asian Office of Aerospace Research and Development (AOARD 114057), International Technology Center–Pacific, and a Ramanujan fellowship from the Department of Science and Technology, Government of India (to S.P.S.).

Notes

This article is a PNAS Direct Submission.

Authors

Affiliations

Tanvi Deora
National Centre for Biological Sciences, Tata Institute of Fundamental Research, Bangalore 560065, India
Amit Kumar Singh
National Centre for Biological Sciences, Tata Institute of Fundamental Research, Bangalore 560065, India
Sanjay P. Sane1 [email protected]
National Centre for Biological Sciences, Tata Institute of Fundamental Research, Bangalore 560065, India

Notes

1
To whom correspondence should be addressed. Email: [email protected].
Author contributions: T.D. and S.P.S. designed research; T.D. and A.K.S. performed research; T.D., A.K.S., and S.P.S. analyzed data; and T.D. and S.P.S. wrote the paper.

Competing Interests

The authors declare no conflict of interest.

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    Biomechanical basis of wing and haltere coordination in flies
    Proceedings of the National Academy of Sciences
    • Vol. 112
    • No. 5
    • pp. 1239-1641

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