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Jack-of-all-trades master of all? Snake vertebrae have a generalist inner organization

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Abstract

Snakes are a very speciose group of squamates that adapted to various habitats and ecological niches. Their ecological diversity is of particular interest and functional demands associated with their various styles of locomotion are expected to result in anatomical specializations. In order to explore the potential adaptation of snakes to their environment we here analyze variation in vertebral structure at the microanatomical level in species with different locomotor adaptations. Vertebrae, being a major element of the snake body, are expected to display adaptations to the physical constraints associated with the different locomotor modes and environments. Our results revealed a rather homogenous vertebral microanatomy in contrast to what has been observed for other squamates and amniotes more generally. We here suggest that the near-absence of microanatomical specializations in snake vertebrae might be correlated to their rather homogeneous overall morphology and reduced range of morphological diversity, as compared to lizards. Thus, snakes appear to retain a generalist inner morphology that allows them to move efficiently in different environments. Only a few ecologically highly specialized taxa appear to display some microanatomical specializations that remain to be studied in greater detail.

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References

  • Abramoff MD, Magelhaes PJ, Ram SJ (2004) Image processing with image J. Biophoton Int 11:36–42

    Google Scholar 

  • Aerts P, Van Damme R, Vanhooydonck B, Zaaf A, Herrel A (2000) Lizard locomotion: how morphology meets ecology. Neth J Zool 50:261–277

    Google Scholar 

  • Aubret F (2004) Aquatic locomotion and behaviour in two disjunct populations of western Australian tiger snakes, Notechis ater occidentalis. Aust J Zool 52:357–368

    Article  Google Scholar 

  • Aubret F, Bonnet X, Shine R (2007) The role of adaptive plasticity in a major evolutionary transition: early aquatic experience affects locomotor performance of terrestrial snakes. Funct Ecol 21:1154–1161

    Article  Google Scholar 

  • Bickel R, Losos JB (2002) Patterns of morphological variation and correlates of habitat use in chameleons. Biol J Linn Soc 76:91–103

    Article  Google Scholar 

  • Blomberg SP, Garland T Jr, Ives AR (2003) Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57:717–745

    PubMed  Google Scholar 

  • Bonnet X, Ineich I, Shine R (2005) Terrestrial locomotion in sea snakes: the effects of sex and species on cliff-climbing ability in sea kraits (Serpentes, Elapidae, Laticauda). Biol J Linn Soc 85:433–441

    Google Scholar 

  • Canoville A, Laurin M (2010) Evolution of humeral microanatomy and lifestyle in amniotes, and some comments on palaeobiological inferences. Biol J Linn Soc 100:384–406

    Article  Google Scholar 

  • Cohn MJ, Tickle C (1999) Developmental basis of limblessness and axial patterning in snakes. Nature 399:474–479

    Article  CAS  PubMed  Google Scholar 

  • Cubo J (2004) Pattern and process in constructional morphology. Evol Dev 6:131–133

    Article  PubMed  Google Scholar 

  • Cubo J, Legendre P, de Ricqlès A, Montes L, de Margerie E, Castanet J, Desdevises Y (2008) Phylogenetic, functional, and structural components of variation in bone growth rate of amniotes. Evolution & Development 10:217–227

    Article  Google Scholar 

  • de Buffrénil V, Bardet N, Pereda Suberbiola X, Bouya B (2008) Specialization of bone structure in Pachyvaranus crassispondylus Arambourg, 1952, an aquatic squamate from the Late Cretaceous of the southern Tethyan margin. Lethaia 41:59–69

    Article  Google Scholar 

  • Dumont M, Laurin M, Jacques F, Pellé E, Dabin W, de Buffrénil V (2013) Inner architecture of vertebral centra in terrestrial and aquatic mammals: a two-dimensional comparative study. J Morphol. doi:10.1002/jmor.20122

    PubMed  Google Scholar 

  • Gans C (1986) Locomotion of limbless vertebrates: pattern and evolution. Herpetologica 42:33–46

    Google Scholar 

  • Gans C (1994) Approaches to the evolution of limbless locomotion. Cuad Herpetol 8:12–17

    Google Scholar 

  • Garland TJ, Losos JB (1994) Ecological morphology of locomotor performance in squamate reptiles. In: Wainwright PC, Reilly S (eds) Ecological morphology: integrative organismal biology. University of Chicago Press, Chicago, pp 240–302

    Google Scholar 

  • Garland T Jr, Harvey PH, Ives AR (1992) Procedures for the analysis of comparative data using phylogenetically independent contrasts. Syst Biol 41:18–32

    Google Scholar 

  • Garland T Jr, Dickerman AW, Janis CM, Jones JA (1993) Phylogenetic analysis of covariance by computer simulation. Syst Biol 42:265–292

    Google Scholar 

  • Gasc JP (1976) Snake vertebrae-a mechanism or merely a taxonomist's toy? In: Bellairs AdA, Cox CB (eds) Mophology and Biology of Reptiles, Vol. 3, Linnean Society Symposium Series, pp. 177–190

  • Gasc JP (1977) Morphologie vertébrale et mode de locomotion chez les squamates: supériorité de l'analyse morpho-fonctionnelle sur la morphologie descriptive. Bulletin Biologique de la France et de la Belgique 111:29–44

    Google Scholar 

  • Gould SJ (2002) The structure of evolutionary theory. The Belknap Press of Harvard University Press, Cambridge

    Google Scholar 

  • Hayashi S, Houssaye A, Nakajima Y, Chiba K, Inuzuka N, Sawamura H, Ando T, Osaki T, Kaneko N (2013) Bone histology suggests increasing aquatic adaptations in Desmostylia (Mammalia, Afrotheria). Plos One 8:e59146

    Article  CAS  PubMed  Google Scholar 

  • Herrel A, Vanhooydonck B, Porck J, Irschick DJ (2008) Anatomical basis of differences in locomotor behavior in Anolis lizards: a comparison between two ecomorphs. Bull Mus Comp Zool 159:213–238

    Article  Google Scholar 

  • Houssaye A (2009) “Pachyostosis” in aquatic amniotes: a review. Integrative Zoology 4:325–340

    Article  PubMed  Google Scholar 

  • Houssaye A (2013) Paleoecological and morphofunctional interpretation of bone mass increase: an example in late cretaceous shallow marine squamates. Biol Rev 88:117–139

    Article  PubMed  Google Scholar 

  • Houssaye A, Bardet N (2012) Ribs and vertebrae microanatomical characteristics in hydropelvic mosasauroids. Lethaia 45:200–209

    Article  Google Scholar 

  • Houssaye A, Mazurier A, Herrel A, Volpato V, Tafforeau P, Boistel R, de Buffrénil V (2010) Vertebral microanatomy in squamates: structure, growth and ecological correlates. J Anat 217:715–727

    Article  PubMed  Google Scholar 

  • Irschick DJ, Garland TJ (2001) Integrating function and ecology in studies of adaptation: investigations of locomotor capacity as a model system. Annu Rev Ecol Syst 32:367–396

    Article  Google Scholar 

  • Irschick DJ, Austin CC, Petren K, Fisher RN, Losos JB, Ellers O (1996) A comparative analysis of clinging ability among pad-bearing lizards. Biol J Linn Soc 59:21–35

    Article  Google Scholar 

  • Jayne BC (1982) Comparative morphology of the semispinalis-spinalis muscle of snakes and correlations with locomotion and constriction. J Morphol 172:83–96

    Article  Google Scholar 

  • Jayne BC (1986) Kinematics of terrestrial snake locomotion. Copeia 4:915–927

    Article  Google Scholar 

  • Johnson RG (1955) The adaptative and phylogenetic significance of vertebral form in snakes. Evolution 9:367–388

    Article  Google Scholar 

  • Lawson R, Slowinski J, Crother BI, Burbrink F (2005) Phylogeny of the Colubroidea (Serpentes): new evidence from mitochondrial and nuclear genes. Mol Phylogenet Evol 37:581–601

    Article  CAS  PubMed  Google Scholar 

  • Lee MSY, Scanlon JD (2002) Snake phylogeny based on osteology, soft anatomy and ecology. Biol Rev 77:333–401

    Article  PubMed  Google Scholar 

  • Lillywhite HB, LaFrentz JR, Lin YC, Tu MC (2000) The cantilever abilities of snakes. J Herpetol 34:523–528

    Article  Google Scholar 

  • Liu XS, Bevill G, Keaveny TM, Sajda P, Guo XE (2009) Micromechanical analyses of vertebral trabecular bone based on individual trabeculae segmentation of plates and rods. J Biomech 42:249–256

    Article  PubMed  Google Scholar 

  • Losos JB (1994) Integrative approaches to evolutionary ecology: Anolis lizards as model systems. Annu Rev Ecol Syst 25:467–493

    Article  Google Scholar 

  • Losos JB, Warheit KI, Schoener TW (1997) Adaptive differentiation following experimental island colonization in Anolis lizards. Nature 387:70–73

    Article  CAS  Google Scholar 

  • Luke C (1986) Convergent evolution of lizard toe fringes. Biol J Linn Soc 27:1–16

    Article  Google Scholar 

  • Mattison C (2008) Tous les serpents du monde. Delachaux et Niestlé

  • McElroy EJ, Reilly SM (2009) The relationship between limb morphology, kinematics, and force during running: the evolution of locomotor dynamics in lizards. Biol J Linn Soc 97:634–651

    Article  Google Scholar 

  • Moon BR (1999) Testing an inference of function from structure: snake vertebrae do the twist. J Morphol 241:217–225

    Article  CAS  PubMed  Google Scholar 

  • Murphy JC (2012) Marine invasions by non-sea snakes, with thoughts on terrestrial–aquatic–marine transitions. Integr Comp Biol 52:217–226

    Article  PubMed  Google Scholar 

  • Pianka E, King D (2004) Varanoid lizards of the world. Indiana University Press

  • Rawlings LH, Rabosky DL, Donnellan SC, Hutchinson MN (2008) Python phylogenetics: inference from morphology and mitchondrial DNA. Biol J Linn Soc 93:603–619

    Article  Google Scholar 

  • Rohlf FJ (2006) A comment on phylogenetic correction. Evolution 60:1509–1515

    Article  PubMed  Google Scholar 

  • Ruimerman R, Bv R, Hilbers P, Huiskes R (2005) The effects of trabecular-bone loading variables on the surface signaling potential for bone remodeling and adaptation. Ann Biomed Eng 33:71–78

    Article  CAS  PubMed  Google Scholar 

  • Sanders KL, Rasmussen AR, Elmberg J (2012) Independent innovation in the evolution of paddle-shaped tails in viviparous sea snakes (Elapidae: Hydrophiinae). Integr Comp Biol 52:311–320

    Article  PubMed  Google Scholar 

  • Seilacher A (1970) Arbeitskonzept zur konstruktions-morphologie. Lethaia 3:393–396

    Article  Google Scholar 

  • Smith TL, Povel GDE, Kardong KV (2002) Predatory strike of the tentacled snake (Erpeton tentaculatum). J Zool 256:233–242

    Article  Google Scholar 

  • Tafforeau P, Boistel R, Boller R, Bravin A, Brunet M, Chaimanee Y, Cloetens P, Feist M, Hoszowska J, Jaeger J-J, Kay RF, Lazzari V, Marivaux L, Nel A, Nemoz C, Thibault X, Vignaud P, Zabler S (2006) Applications of X-ray synchrotron microtomography for non-destructive 3D studies of paleontological specimens. Appl Phys A 83:195–202

    Google Scholar 

  • Turner CH (1998) Three rules for bone adaptation to mechanical stimuli. Bone 23:399–407

    Article  CAS  PubMed  Google Scholar 

  • Van Damme R, Vanhooydonck B, Aerts P, De Vree F (2003) Evolution of lizard locomotion: context and constraint. In: Bels VL, Gasc J-P, Casinos A (eds) Vertebrate biomechanics and evolution, vol 16. BIOS, Oxford, pp 267–282

    Google Scholar 

  • Vanhooydonck B, Van Damme R (2001) Evolutionary trade-offs in locomotor capacities in lacertid lizards: are splendid sprinters clumsy climbers? J Evol Biol 14:46–54

    Article  Google Scholar 

  • Vincent SE, Herrel A, Irschick DJ (2005) Comparisons of aquatic versus terrestrial predatory strikes in the pitviper, Agkistrodon piscivorus. J Exp Zool 303:476–488

    Article  Google Scholar 

  • Walton M, Jayne BC, Bennett AF (1990) The energetic cost of limbless locomotion. Science 249:524–527

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We warmly thank R. Lebrun (Institut des Sciences de l’Evolution, Université Montpellier 2, Montpellier, France) and the Montpellier RIO Imaging (MRI) platform for giving access to their imaging facilities, the ESRF (Grenoble, France) for providing beamtime and support, G. Daghfous (Laboratoire de Réjean DUBUC, Université de Montréal, Canada) for the realization of some scans, I. Ineich (Muséum National d’Histoire Naturelle, Paris, France) for the loan of some specimens, and A.C. Fabre (University College London, United Kingdom) for her help with statistics. We are also thankful to three anonymous reviewers for fruitful comments that improved the manuscript , and to S. Thatje for editorial work. Al. H. acknowledges financial support from the A. v. Humboldt Foundation.

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Correspondence to Alexandra Houssaye.

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Communicated by: Sven Thatje

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Houssaye, A., Boistel, R., Böhme, W. et al. Jack-of-all-trades master of all? Snake vertebrae have a generalist inner organization. Naturwissenschaften 100, 997–1006 (2013). https://doi.org/10.1007/s00114-013-1102-x

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  • DOI: https://doi.org/10.1007/s00114-013-1102-x

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