Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Wing upstroke and the evolution of flapping flight

Nature volume 387, pages 799–802 (1997)Cite this article

Abstract

Movements of the wing during upstroke in birds capable of powered flight are more complex than those of downstroke1,2,3. The m. supracoracoideus (SC) is a muscle with a highly derived morphology that is generally considered to be the primary elevator of the wing4,5,6. This muscle arises from the ventrally oriented sternum and its tendon of insertion passes craniodorsally through a special bony canal, around a bony process which deflects it laterally, to attach on the dorsal aspect of the humerus above the glenohumeral joint (Fig. 1). We studied the contractile properties of the SC in situ and related them to wing kinematics in the European starling (Sturnus vulgaris). Our findings indicate that the primary role of the SC is to impart a high-velocity rotation about the longitudinal axis of the humerus. This rapid ‘twisting’ of the humerus, coupled with limited humeral elevation, is responsible for positioning the forearm and hand so that their subsequent extension orients the outstretched wing appropriately for the following downstroke. This reinterpretation of the primary function of the SC provides insight into the selective advantage of its unique musculoskeletal organization in the evolution of powered flapping flight in birds.

The m. pectoralis has been removed, as well as all other wing and shoulder musculature to expose the m. supracoracoideus (SC) and its tendon of insertion on the dorsal aspect of the humerus. The fascicles of the SC arise from the dorsal half of the carina, the adjacent body of the sternum, and a small area on the base of the coracoclavicular membrane. The SC's bipinnate architecture limits tendon excursion but maximizes force production. Scale bar, 1.0cm. Abbreviations: SCA, scapula; HUM, humerus; COR, coracoid; TC, triosseal canal; FUR, furcula, STR, sternum.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 2: Rotational force of the m.
Figure 3: Functional correlates of length–force in European starlings (Sturnus vulgaris).

Similar content being viewed by others

References

  1. Brown, R. H. J. Flapping flight. Ibis 93, 333–359 (1951).

    Article  Google Scholar 

  2. Dial, K. P., Goslow, G. E. J & Jenkins, F. A. J The functional anatomy of the shoulder in the European starling (Sturnus vulgaris). J. Morphol. 207, 327–344 (1991).

    Article  Google Scholar 

  3. Simpson, S. F. The flight mechanism of the pigeon Columba livia during take-off. J. Zool. 200, 435–443 (1983).

    Article  Google Scholar 

  4. Dial, K. P., Kaplan, S. R., Goslow, G. E. J & Jenkins, F. A. J Afunctional analysis of the primary upstroke and downstroke muscles in the domestic pigeon (Columba livia) during flight. J. Exp. Biol. 134, 1–16 (1988).

    CAS  PubMed  Google Scholar 

  5. Norberg, U. M. Vertebrate Flight 1–291 (Springer, Berlin, (1989)).

    Google Scholar 

  6. Rayner, J. M. V. The evolution of vertebrate flight. Biol. J. Linn. Soc. 34, 269–287 (1988).

    Article  Google Scholar 

  7. Spedding, G. R., Rayner, J. M. V. & Pennycuick, C. J. Momentum and energy in the wake of a pigeon (Columba livia) in slow flight. J. Exp. Biol. 111, 81–102 (1984).

    Google Scholar 

  8. Ostrom, J. H. Archaeopteryx and the origin of birds. Biol. J. Linn. Soc. 8, 91–182 (1976).

    Article  Google Scholar 

  9. Ostrom, J. H. Some hypothetical anatomical stages in the evolution of avian flight. Smithson. Contr. Paleobiol. 27, 1–21 (1976).

    Google Scholar 

  10. Sanz, J. L. et al. An Early Cretaceous bird from Spain and its implications for the evolution of avian flight. Nature 382, 442–445 (1996).

    Article  ADS  CAS  Google Scholar 

  11. Hou, L., Zhou, Z., Martin, L. D. & Feduccia, A. Abeaked bird from the Jurassic of China. Nature 377, 616–618 (1995).

    Article  ADS  Google Scholar 

  12. Chiappe, L. M. & Calvo, J. O. Neuquenornis volans, a new Late Cretaceous bird (Enantiornithes: Avisuridae) from Patagonia, Argentina. J. Vert. Paleo. 14, 230–246 (1994).

    Article  Google Scholar 

  13. Hou, L. Alate mesozoic bird from inner Mongolia. Vert. Pal Asiatica 32, 258–266 (1994).

    Google Scholar 

  14. Sereno, P. C. & Rao, C. Early evolution of avian flight and perching: New evidence from the Lower Cretaceous of China. Science 255, 845–848 (1992).

    Article  ADS  CAS  Google Scholar 

  15. Zhou, Z., Jin, F. & Zhang, J. Preliminary report on a Mesozoic bird from Liaoning, China. Chinese Sci. Bull. 37 (16), 1365–1368 (1992).

    Google Scholar 

  16. Olson, S. L. & Feduccia, A. Flight capability and the pectoral girdle of Archaeopteryx. Nature 278, 247–248 (1979).

    Article  ADS  Google Scholar 

  17. Rayner, J. M. V. in Biomechanics in Evolution(eds Rayner, J. M. V. & Wootton, R. J.) 183–212 (Cambridge Univ. Press, (1991)).

    Google Scholar 

  18. Rayner, J. M. V. Form and function in avian flight. Curr. Ornithol. 5, 1–77 (1988).

    Google Scholar 

  19. Meyers, R. A. Gliding flight in the American kestrel (Falco sparverius): An electromyographic study. J. Morphol. 215, 213–224 (1993).

    Article  Google Scholar 

  20. Tobalske, B. W. & Dial, K. P. Neuromuscular control and kinematics of intermittent flight in budgerigars (Melopstittacus undulatus). J. Exp. Biol. 187, 1–18 (1994).

    CAS  PubMed  Google Scholar 

  21. Spector, S. A., Gardiner, P. F., Zernicke, R. Z., Roy, R. R. & Edgerton, V. R. Muscle architecture and force-velocity characteristics of cat soleus and medial gastrocnemius: Implications for motor control. J. Neurophysiol. 44, 951–960 (1980).

    Article  CAS  Google Scholar 

  22. Cohen, A. H., Rossignol, S. & Grillner, S. Neural Control of Rhythmic Movements in Vertebrates 1–500 (Wiley, New York, (1988)).

    Google Scholar 

  23. Jenkins, F. A. J The evolution of the avian shoulder joint. Am. J. Sci. 293A, 253–367 (1993).

    Article  ADS  Google Scholar 

  24. Sy, M. Funktionell-anatamische Untersuchungen am Vogelflügel. J. Ornithol. 84, 253–267 (1936).

    Article  Google Scholar 

  25. Hazelhurst, G. A. & Rayner, J. M. V. An unusual flight mechanism in the pterosauria. Paleontology 35, 927–941 (1992).

    Google Scholar 

  26. Wellnhofer, P. in Archaeopteryx 1–30 Ein neues Exemples von Archaeopteryr(Freunde des Jura-Museums Eichstätt, (1988)).

    Google Scholar 

  27. Wellnhofer, P. in Archaeopteryx 1–47 Das siebte Exemplar von Archaeosteryx aus den Solnhofener Schichten. (Freunde des Jure-Museums Eichstätt, (1993)).

    Google Scholar 

  28. Sanz, J. L., Chiappe, L. M. & Buscalioni, A. D. The osteology of Concornis lacustris (Aves: Enantiornithes) from the lower Cretaceous of Spain and a reexamination of its phylogenetic relationships. Novitates 3133, 1–23 (1995).

    Google Scholar 

  29. Kurochkin, E. N. Atrue carinate bird from Lower Cretaceous deposits in Mongolia and other evidence of Early Cretaceous birds in Asia. Cretaceous Res. 6, 271–278 (1985).

    Article  Google Scholar 

  30. Sanz, J. L. & Bonaparte, J. F. Anew order of birds (class Aves) from the Lower Cretaceous (Spain). Nat. Hist. Mus. L.A. County Sci. Ser. 36, 39–49 (1992).

    Google Scholar 

Download references

Acknowledgements

We thank L. Chiappe, K. Earls, J. Gray-Chickering, C. Kovacs, F. A. Jenkins Jr, D.Ritter, J. Ostrom and T. A. McMahon for critically reviewing the manuscript and for their encouragement; M. Morimoto and A. Valore for technical assistance; and L. L. Meszoely and K.Brown-Wing for Figs 1 and 3, and Fig. 2, respectively. This work was supported by a grant from the NSF.

Author information

Authors and Affiliations

  1. Department of Ecology and Evolutionary Biology, Brown University, Providence, 02912, Rhode Island, USA

    Samuel O. Poore, A. Sánchez-Haiman & G. E. Goslow Jr

Authors
  1. Samuel O. Poore
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. Sánchez-Haiman
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. G. E. Goslow Jr
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Samuel O. Poore.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Poore, S., Sánchez-Haiman, A. & Goslow, G. Wing upstroke and the evolution of flapping flight. Nature 387, 799–802 (1997). https://doi.org/10.1038/42930

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/42930

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing