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A fundamental avian wing-stroke provides a new perspective on the evolution of flight

Nature volume 451, pages 985–989 (2008)Cite this article

Abstract

The evolution of avian flight remains one of biology’s major controversies, with a long history of functional interpretations of fossil forms given as evidence for either an arboreal or cursorial origin of flight. Despite repeated emphasis on the ‘wing-stroke’ as a necessary avenue of investigation for addressing the evolution of flight1,2,3,4, no empirical data exist on wing-stroke dynamics in an experimental evolutionary context. Here we present the first comparison of wing-stroke kinematics of the primary locomotor modes (descending flight and incline flap-running) that lead to level-flapping flight in juvenile ground birds throughout development (Fig. 1). We offer results that are contrary both to popular perception and inferences from other studies5,6,7. Starting shortly after hatching and continuing through adulthood, ground birds use a wing-stroke confined to a narrow range of less than 20°, when referenced to gravity, that directs aerodynamic forces about 40° above horizontal, permitting a 180° range in the direction of travel. Based on our results, we put forth an ontogenetic-transitional wing hypothesis that posits that the incremental adaptive stages leading to the evolution of avian flight correspond behaviourally and morphologically to transitional stages observed in ontogenetic forms.

Our data suggest a default or basal wing-stroke is used by young and adults and may exist in all birds (Supplementary Videos). The fundamental wing-stroke described herein is used days after hatching and during all ages and over multiple behaviours (that is, flap-running, descending and level flight) and is the foundation of our new ontogenetic-transitional wing hypothesis. At hatching, chicks can ascend inclines as steep as 60° by crawling on all four limbs. From day 8 through adulthood, birds use a consistently orientated stroke-plane angle over all substrate inclines during wing-assisted incline running (red arcs) as well as during descending and level flight (blue arcs). Estimated force orientations from this conserved wing-stroke are limited to a narrow wedge (see Fig. 3b).

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Figure 2: Average stroke-plane angle among locomotor styles in three frames of reference.
Figure 3: Comparison of wing-stroke plane angle, estimated force orientation and angle of attack among locomotor styles.

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References

  1. Gauthier, J. A. & Padian, K. in The Beginnings of Birds: Proc. Int. Archaeopteryx Conf., Eichstatt 1984 (eds Hecht, M. K., Ostrom, J. H., Viohl, G. & Wellnhofer, P.) 185–197 (Freunde des Jura-Museums, Eichstatt, West Germany, 1985)

    Google Scholar 

  2. Padian, K. The origins and aerodynamics of flight in extinct vertebrates. Paleontology 28, 413–433 (1985)

    Google Scholar 

  3. Padian, K. & Chiappe, L. M. The origin of birds and their flight. Sci. Am. 278, 38–47 (1998)

    Article  CAS  Google Scholar 

  4. Padian, K. in New Perspectives on the Origin and Early Evolution of Birds. Proc. Int. Symp. in Honor of J. H. Ostrom (eds Gauthier, J. A. & Gall, L. F.) 255–272 (Special Publication of the Peabody Museum of Natural History, New Haven, 2001)

    Google Scholar 

  5. Tobalske, B. W. & Dial, K. P. Flight kinematics of black-billed magpies and pigeons over a wide range of speeds. J. Exp. Biol. 199, 263–280 (1996)

    CAS  PubMed  Google Scholar 

  6. Hedrick, T. L., Tobalske, B. W. & Biewener, A. A. Estimates of circulation and gait change based on a three-dimensional kinetic analysis of flights in cockatiels (Nymphicus hollandicus) and ringed turtle-doves (Streptopelia risoria). J. Exp. Biol. 205, 1389–1409 (2002)

    PubMed  Google Scholar 

  7. Park, K. J., Rosén, M. & Hedenström, A. Flight kinematics of the barn swallow (Hirundo rustica) over a wide range of speeds in a wind tunnel. J. Exp.Biol. 204, 2741–2750 (2001)

    CAS  PubMed  Google Scholar 

  8. Dial, K. P. Wing-assisted incline running and the evolution of flight. Science 299, 402–404 (2003)

    Article  ADS  CAS  Google Scholar 

  9. Bundle, M. W. & Dial, K. P. Mechanics of wing-assisted incline running (WAIR). J. Exp. Biol. 206, 4553–4564 (2003)

    Article  Google Scholar 

  10. Dial, K. P., Randall, R. J. & Dial, T. R. What use is half a wing in the ecology and evolution of birds? Bioscience 56, 437–445 (2006)

    Article  Google Scholar 

  11. Tobalske, B. W. & Dial, K. P. Aerodynamics of wing-assisted incline running in birds. J. Exp. Biol. 210, 1742–1751 (2007)

    Article  Google Scholar 

  12. Chiappe, L. M. Glorified Dinosaurs: The Origin and Early Evolution of Birds (Wiley, New York, 2007)

    Google Scholar 

  13. Witmer, L. M. in Mesozoic Birds: Above the Heads of Dinosaurs (eds Witmer, L. M. & Chiappe, L. M.) 3–30 (Univ. California Press, Berkeley, 2002)

    Google Scholar 

  14. Gatesy, S. M. & Baier, D. B. The origin of the avian flight stroke: a kinematic and kinetic perspective. Paleobiology 31, 382–399 (2005)

    Article  Google Scholar 

  15. Sibley, C. G. & Ahlquist, J. E. Phylogeny and Classification of Birds, a Study in Molecular Evolution (Yale Univ. Press, New Haven, 1990)

    Google Scholar 

  16. Warrick, D. R. & Dial, K. P. Kinematic, aerodynamic and anatomical mechanisms in the slow, maneuvering flight of pigeons. J. Exp. Biol. 201, 655–672 (1998)

    PubMed  Google Scholar 

  17. Hedrick, T. L. & Biewener, A. A. Low speed maneuvering flight of the rose-breasted cockatoo (Eolophus roseicapillus) I. Kinematic and neuromuscular control of turning. J. Exp. Biol. 210, 1897–1911 (2007)

    Article  CAS  Google Scholar 

  18. Feduccia, A. & Tordoff, H. B. Feather of Archaeopteryx: asymmetric vanes indicate aerodynamic function. Science 203, 1021–1022 (1979)

    Article  ADS  CAS  Google Scholar 

  19. Norberg, U. M. in The Beginnings of Birds: Proc. Int. Archaeopteryx Conf., Eichstatt 1984 (eds Hecht, M. K., Ostrom, J. H., Viohl, G. & Wellnhofer, P.) 293–302 (Freunde des Jura-Museums, Eichstatt, West Germany, 1985)

    Google Scholar 

  20. Norberg, R. A. in The Beginnings of Birds: Proc. Int. Archaeopteryx Conf., Eichstatt 1984 (eds Hecht, M. K., Ostrom, J. H., Viohl, G. & Wellnhofer, P.) 303–318 (Freunde des Jura-Museums, Eichstatt, West Germany, 1985)

    Google Scholar 

  21. Speakman, J. R. & Thomson, S. C. Feather asymmetry in Archaeopteryx. Nature 374, 221–222 (1995)

    Article  ADS  CAS  Google Scholar 

  22. Garner, J. P., Taylor, G. K. & Thomas, A. L. R. On the origins of birds: the sequence of character acquisition in the evolution of avian flight. Proc. R. Soc. Lond. B 266, 1259–1266 (1999)

    Article  Google Scholar 

  23. Paul, G. S. Dinosaurs of the Air (Johns Hopkins Univ. Press, Baltimore, 2002)

    Google Scholar 

  24. Segre, P. & Dial, K. P. Half a wing in motion: the ontogeny and wing kinematics of WAIR in chukars. Int. Comp. Biol. 45, 1191 P2.48. (2006)

    Google Scholar 

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

    Google Scholar 

  26. Jenkins, F. A. The evolution of the avian shoulder joint. Am. J. Sci. 293, 253–267 (1993)

    Article  ADS  Google Scholar 

  27. Xu, X. et al. Basal tyrannosauroids from China and evidence for protofeathers in tyrannosauroids. Nature 431, 680–684 (2004)

    Article  ADS  CAS  Google Scholar 

  28. Padian, K. & Dial, K. P. Origin of flight: could ‘four-winged’ dinosaurs fly? Nature 438, E3 (2005)

    Article  ADS  CAS  Google Scholar 

  29. Jones, T. D., Farlow, J. O., Ruben, A., Henderson, D. H. & Hillenius, W. J. Cursoriality in bipedal archosaurs. Nature 406, 716–718 (2000)

    Article  ADS  CAS  Google Scholar 

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Acknowledgements

We thank the following for their suggestions and comments: A. Biewener, M. Bundle, R. Callaway, H. Davis, S. Gatesy, D. Irschick, F. Jenkins, Jr, J. Maron, T. Martin, K. Padian and B. Tobalske.

Author Contributions K.P.D. provided the conceptual foundation, funding and facilities. K.P.D. and B.E.J. wrote the manuscript. B.E.J. and P.S. performed most data acquisition and analyses.

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  1. Division of Biological Sciences, Flight Laboratory, University of Montana, 32 Campus Drive, Missoula, Montana 59812, USA,

    Kenneth P. Dial, Brandon E. Jackson & Paolo Segre

Authors
  1. Kenneth P. Dial
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  3. Paolo Segre
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Corresponding author

Correspondence to Kenneth P. Dial.

Supplementary information

Supplementary Information 1

The file contains Supplementary Figures S1-S2, Supplementary Methods and Legends to Supplementary Videos 1-4. (PDF 935 kb)

Supplementary Information 2

This file contains Supplementary Video 1. (MOV 2755 kb)

Supplementary Information 3

This file contains part one of the Supplementary Video 2. (MOV 10077 kb)

Supplementary Information 4

This file contains part two of the Supplementary Video 2. (MOV 6616 kb)

Supplementary Information 5

This file contains part one of the Supplementary Video 3. (MOV 9237 kb)

Supplementary Information 6

This file contains part two of the Supplementary Video 3. (MOV 2469 kb)

Supplementary Information 7

This file contains part one of the Supplementary Video 4. (MOV 13143 kb)

Supplementary Information 8

This file contains part two of the Supplementary Video 4. (MOV 8722 kb)

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Dial, K., Jackson, B. & Segre, P. A fundamental avian wing-stroke provides a new perspective on the evolution of flight. Nature 451, 985–989 (2008). https://doi.org/10.1038/nature06517

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