Movement in a gravitational field: The question of limb interarticular coordination in terrestrial vertebrates

  • Pierre Legreneur
  • Vincent Bels
  • Karine Monteil
  • Michel Laurin
Regular Article
Part of the following topical collections:
  1. Physical constraints of morphogenesis and evolution

Abstract

In this paper, we demonstrated that interarticular coordination of terrestrial tetrapods emerges from an environment highly constrained by friction and the gravitational field. We briefly review recent works on the jumping behavior in squamates, lemurs and amphibians. We then explore previously published work as well as some unpublished experimental data on human jumping. Finally, we end by inferring locomotion in some of the first limbed vertebrates using a simulation procedure. All these data show that despite changes in shape, structure, and motor controls of taxa, the same spatio-temporal sequence of joint displacements always occurs when the movement is executed in a terrestrial environment. Comparison with aquatic locomotion argues for the hypothesis that this pattern emerged in early terrestrial tetrapods as a response to the gravitational constraint and the terrestrial frictional environment.

Graphical abstract

Keywords

Topical issue: Physical constraints of morphogenesis and evolution 

References

  1. 1.
    S. Gursky, K. Nekaris Primate Anti-Predator Strategies (Springer, 2007).Google Scholar
  2. 2.
    J.B. Losos Ecology and Adaptive Radiation of Anoles: Lizards in an Evolutionary Tree (University of California Press, Berkeley and Los Angeles, California, 2009).Google Scholar
  3. 3.
    S.J. Arnold, Am. Zool. 23, 347 (1983).Google Scholar
  4. 4.
    G. Goslow Jr., D. Wilson, S.O. Poore, Brain, Behav. Evolut. 55, 85 (2000).CrossRefGoogle Scholar
  5. 5.
    G. Lauder, in Biomechanics in Evolution (1991) pp. 1-19.Google Scholar
  6. 6.
    M. Jamon, in How Vertebrates Moved Onto Land (Muséum National d’Histoire Naturelle, Paris, 2011) pp. 171-185.Google Scholar
  7. 7.
    J.R. Fetcho, Brain, Behav. Evolut. 40, 82 (1992).CrossRefGoogle Scholar
  8. 8.
    A.B. Butler, W. Hodos, Comparative Vertebrate Neuroanatomy: Evolution and Adaptation (Wiley Online Library, 1996).Google Scholar
  9. 9.
    W. Hennig, Phylogenetic Systematics (University of Illinois Press, Urbana, Chicago, London, 1966).Google Scholar
  10. 10.
    M. Laurin, in Evolutionary Biology - Concepts, Biodiversity, Macroevolution and Genome Evolution (Springer, Berlin, 2011) pp. 121-138.Google Scholar
  11. 11.
    W. Maddison, M. Slatkin, Syst. Biol. 39, 175 (1990).Google Scholar
  12. 12.
    G. Didier, Bull. Math. Biol. 73, 1477 (2011).MathSciNetCrossRefMATHGoogle Scholar
  13. 13.
    W.P. Maddison, Syst. Biol. 40, 304 (1991).CrossRefGoogle Scholar
  14. 14.
    J. Felsenstein, Syst. Biol. 22, 240 (1973).CrossRefGoogle Scholar
  15. 15.
    J. Felsenstein, Am. Nat. 125, 1 (1985).CrossRefGoogle Scholar
  16. 16.
    E.P. Martins, T.F. Hansen, Am. Nat. 149, 646 (1997).CrossRefGoogle Scholar
  17. 17.
    Y. Desdevises, P. Legendre, L. Azouzi, S. Morand, Evolution 57, 2647 (2003).Google Scholar
  18. 18.
    A.F. Read, S. Nee, J. Theor. Biol. 173, 99 (1995).CrossRefGoogle Scholar
  19. 19.
    W.P. Maddisson, J. Theor. Biol. 202, 195 (2000).CrossRefGoogle Scholar
  20. 20.
    S.B. Hedges, S. Kumar, The Timetree of Life (Oxford University Press, Oxford, 2009).Google Scholar
  21. 21.
    F. Gomes, E. Rezende, M. Grizante, C. Navas, J. Evol. Biol. 22, 1088 (2009).CrossRefGoogle Scholar
  22. 22.
    D. Marjanovic, M. Laurin, Syst. Biol. 56, 369 (2007).CrossRefGoogle Scholar
  23. 23.
    P. Ward, C. Labandeira, M. Laurin, R.A. Berner, Proc. Natl. Acad. Sci. U.S.A. 103, 16818 (2006).ADSCrossRefGoogle Scholar
  24. 24.
    R. Alexander, Principles of Animal Locomotion (Princeton University Press, Princeton, 2003).Google Scholar
  25. 25.
    R.M. Alexander, Philos. Trans. R. Soc. London, Ser. B 347, 235 (1995).ADSCrossRefGoogle Scholar
  26. 26.
    M.M. Günther, H. Ishida, H.N. Kamakura, Z. Morphol. Anthropol. 78, 341 (1991).Google Scholar
  27. 27.
    S. Nauwelaerts, P. Aerts, J. Exp. Biol. 209, 66 (2006).CrossRefGoogle Scholar
  28. 28.
    G.J. van Ingen Schenau, Hum. Mov. Sci. 3, 301 (1984).CrossRefGoogle Scholar
  29. 29.
    A.A. Biewener, T.J. Roberts, Exercise Sport Sci. Rev. 28, 99 (2000).Google Scholar
  30. 30.
    T.E. Higham, A. Biewener, S.L. Delp, Philos. Trans. R. Soc. London, Ser. B 366, 1463 (2011).CrossRefGoogle Scholar
  31. 31.
    P. Legreneur, F.R. Thévenet, K.M. Monteil, S.J. Montuelle, E. Pouydebat, V. Bels, J. Exp. Biol. 213, 1320 (2010).CrossRefGoogle Scholar
  32. 32.
    P. Legreneur, M. Laurin, K. Monteil, V. Bels, Adapt. Behav. 20, 69 (2012).Google Scholar
  33. 33.
    P. Legreneur, T. Creveaux, V. Bels, Intelli. Control Autom. 2, 39 (2011).Google Scholar
  34. 34.
    M.N. Scholz, K. D’Aout, M.F. Bobbert, P. Aerts, Proc. Biol. Sci. 273, 2177 (2006).CrossRefGoogle Scholar
  35. 35.
    P. Aerts, Philos. Trans. R. Soc. London, Ser. B 353, 1607 (1998).CrossRefGoogle Scholar
  36. 36.
    S. Nauwelaerts, P. Aerts, J. Exp. Biol. 206, 4341 (2003).CrossRefGoogle Scholar
  37. 37.
    R.M. Alexander, Hum. Mov. Sci. 8, 339 (1998).CrossRefGoogle Scholar
  38. 38.
    G.J. van Ingen Schenau, Hum. Mov. Sci. 8, 301 (1989).CrossRefGoogle Scholar
  39. 39.
    M.F. Bobbert, G.J. van Ingen Schenau, J. Biomech. 21, 249 (1988).CrossRefGoogle Scholar
  40. 40.
    J. Van Zandwijk, M.F. Bobbert, M. Munneke, P. Pas, Med. Sci. Sports Exercise 32, 477 (2000).CrossRefGoogle Scholar
  41. 41.
    J. Vanrenterghem, A. Lees, M. Lenoir, P. Aerts, D. De Clercq, Hum. Mov. Sci. 22, 713 (2004).CrossRefGoogle Scholar
  42. 42.
    P. Legreneur, K.M. Monteil, E. Pellé, S. Montuelle, V. Bels, Zoology 114, 247 (2011).CrossRefGoogle Scholar
  43. 43.
    D.J. Irschick, J.B. Losos, Am. Nat. 154, 293 (1999).CrossRefGoogle Scholar
  44. 44.
    S.J. Montuelle, G. Daghfous, V.L. Bels, J. Exp. Zool. Part A Ecol. Genet. Physiol. 309, 563 (2008).CrossRefGoogle Scholar
  45. 45.
    N. Bernstein, The Co-Ordination and Regulation of Movements (Pergamon, New York, 1967).Google Scholar
  46. 46.
    L. Gregoire, H.E. Veeger, P.A. Huijing, G.J. van Ingen Schenau, Int. J. Sports Med. 5, 301 (1984).CrossRefGoogle Scholar
  47. 47.
    R. Jacobs, G.J. van Ingen Schenau, J. Biomech. 25, 953 (1992).CrossRefGoogle Scholar
  48. 48.
    H. Jöris, A. Muyen, G.J. van Ingen Schenau, H. Kemper, J. Biomech. 18, 409 (1985).CrossRefGoogle Scholar
  49. 49.
    C. Putnam, Med. Sci. Sports Exercise 23, 130 (1991).Google Scholar
  50. 50.
    J. Van Der Kamp, J. Sports Sci. 24, 467 (2006).CrossRefGoogle Scholar
  51. 51.
    G.J. van Ingen Schenau, K. Bakker, J. Hum. Mov. Studies 6, 1 (1980).Google Scholar
  52. 52.
    J.J. de Koning, G. de Groot, G.J. van Ingen Schenau, J. Biomech. 24, 137 (1991).CrossRefGoogle Scholar
  53. 53.
    M. Haguenauer, P. Legreneur, K.M. Monteil, J. Biomech. 39, 699 (2006).CrossRefGoogle Scholar
  54. 54.
    M. Haguenauer, P. Legreneur, F. Colloud, K.M. Monteil, J. Hum. Mov. Studies 43, 197 (2002).Google Scholar
  55. 55.
    M. Haguenauer, P. Legreneur, K.M. Monteil, J. Appl. Biomech. 21, 236 (2005).Google Scholar
  56. 56.
    P. Janvier, Early Vertebrates (Clarendon Press Oxford, Oxford, 1996).Google Scholar
  57. 57.
    M. Laurin, Zool. Scripta 35, 667 (2006).CrossRefGoogle Scholar
  58. 58.
    N.H. Shubin, P. Alberch, Evol. Biol. 20, 319 (1986).CrossRefGoogle Scholar
  59. 59.
    N.H. Shubin, E.B. Daeschler, F.A. Jenkins, Nature 440, 764 (2006).ADSCrossRefGoogle Scholar
  60. 60.
    M. Laurin, M. Girondot, A. de Ricqlès, Trends Ecol. Evol. 15, 118 (2000).CrossRefGoogle Scholar
  61. 61.
    M. Laurin, How Vertebrates Left the Water (University of California Press, Berkeley, Los Angeles, London, 2010).Google Scholar
  62. 62.
    M.I. Coates, J.A. Clack, Nature 347, 66 (1990).ADSCrossRefGoogle Scholar
  63. 63.
    S.E. Pierce, J.A. Clack, J.R. Hutchinson, Nature 486, 523 (2012).ADSGoogle Scholar
  64. 64.
    E. Jarvik, Fossils & Strata 40, 1 (1996).Google Scholar
  65. 65.
    O.A. Lebedev, M.I. Coates, Zool. J. Linn. Soc. 114, 307 (1995).CrossRefGoogle Scholar
  66. 66.
    M. Laurin, Evolution 52, 1476 (1998).CrossRefGoogle Scholar
  67. 67.
    P.E. Ahlberg, J.A. Clack, H. Blom, Nature 437, 137 (2005).ADSCrossRefGoogle Scholar
  68. 68.
    M.I. Coates, J.E. Jeffery, M. Ruta, Evol. Devel. 4, 390 (2002).CrossRefGoogle Scholar
  69. 69.
    G. Niedzwiedzki, P. Szrek, K. Narkiewicz, M. Narkiewicz, P.E. Ahlberg, Nature 463, 43 (2010).ADSCrossRefGoogle Scholar
  70. 70.
    T. Creveaux, J. Bastien, C. Villars, P. Legreneur, arXiv preprint arXiv:1207.2627 (2012) http://arxiv.org/abs/1207.2627.
  71. 71.
    R. Grasso, M. Zago, F. Lacquaniti, J. Neurophysiol. 83, 288 (2000).Google Scholar
  72. 72.
    K. D’Aout, P. Aerts, D. De Clercq, K. Schoonaert, E. Vereecke, L. Van Elsacker, Primatologie 4, 191 (2001).Google Scholar
  73. 73.
    F.R. Sarlegna, G.M. Gauthier, C. Bourdin, J.L. Vercher, J. Blouin, Brain Res. Bull. 69, 404 (2006).CrossRefGoogle Scholar
  74. 74.
    M. Kawato, Curr. Opin. Neurobiol. 9, 718 (1999).CrossRefGoogle Scholar
  75. 75.
    G.V. Lauder, E.G. Drucker, Ocean. Engin. IEEE J. 29, 556 (2004).CrossRefGoogle Scholar
  76. 76.
    S. Nauwelaerts, E. Stamhuis, P. Aerts, Animal Biol. 55, 3 (2005).CrossRefGoogle Scholar
  77. 77.
    S. Renous, V. Bels, J. Davenport, Hist. Biol. 14, 1 (2000).CrossRefGoogle Scholar
  78. 78.
    A. Berkowitz, J. Comp. Physiol. A 188, 225 (2002).CrossRefGoogle Scholar
  79. 79.
    A. Berkowitz, J. Neurophysiol. 99, 2887 (2008).CrossRefGoogle Scholar
  80. 80.
    A.C. Gibb, M.A. Ashley-Ross, C.M. Pace, J.H. Long Jr., J. Exp. Zool. Part A: Ecol. Gen. Physiol. 315A, 649 (2011).CrossRefGoogle Scholar
  81. 81.
    S. Renous, J. Davenport, V. Bels, in How Vertebrates Moved Onto Land (Muséum National d’Histoire Naturelle, Paris, 2011) pp. 91-128.Google Scholar
  82. 82.
    A. Canoville, M. Laurin, Biol. J. Linn. Soc. 100, 384 (2010).CrossRefGoogle Scholar
  83. 83.
    F.J. Meunier, M. Laurin, Acta Zool. 93, 88 (2012).CrossRefGoogle Scholar
  84. 84.
    A. Boddy, M. McGowen, C. Sherwood, L. Grossman, M. Goodman, D. Wildman, J. Evol. Biol. 25, 981 (2012).CrossRefGoogle Scholar

Copyright information

© EDP Sciences, SIF, Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Pierre Legreneur
    • 1
    • 2
  • Vincent Bels
    • 2
  • Karine Monteil
    • 1
  • Michel Laurin
    • 3
  1. 1.CRIS EA 647 (P3M)Université de LyonVilleurbanneFrance
  2. 2.UMR 7205 (FORCE), CNRS/MNHNMuséum National d’Histoire NaturelleParisFrance
  3. 3.UMR 7207 (CR2P), CNRS/MNHN/UPMCMuséum National d’Histoire NaturelleParisFrance

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