Skip to main content Accessibility help

The evolution of long bone microstructure and lifestyle in lissamphibians

  • Michel Laurin (a1), Marc Girondot (a2) and Marie-Madeleine Loth (a1)


The compactness profile of femoral cross-sections and body size of 105 specimens of 46 species of lissamphibians was studied to assess the effect of lifestyle (aquatic, amphibious, or terrestrial). Several tests that incorporate phylogenetic information (permutational multiple linear regression incorporating phylogenetic distances, logistic regression using phylogenetic weighting, concentrated-changes tests) show that the return to a fully aquatic lifestyle is associated with an increase in the compactness of the femur and an increase in body size. However, amphibious taxa cannot be distinguished from terrestrial ones solely on the basis of size or compactness. Body size and compactness profile parameters of the femur exhibit a phylogenetic signal (i.e., closely related taxa tend to be more similar to each other than to distantly related taxa).

Mathematical equations obtained from our data by using logistic regression with phylogenetic weighting are used to infer the lifestyle of four early stegocephalians. The results are generally congruent with prevailing paleontological interpretations, which suggests that this method could be applied to infer the lifestyle of early taxa whose lifestyle is poorly understood.



Hide All
Akaike, H. 1974. A new look at the statistical model identification. IEEE Transactions on Automatic Control 19:716723.
Andrews, S. M., and Carroll, R. L. 1991. The order Adelospondyli: Carboniferous lepospondyl amphibians. Transactions of the Royal Society of Edinburgh 82:239275.
Báez, A. M. 1981. Redescription and relationships of Saltenia ibanezi, a late Cretaceous pipid frog from Northwestern Argentina. Ameghiniana 22:127154.
Baez, A. M., and Pugener, L. A. 2003. Ontogeny of a new Palaeogene pipid frog from southern South America and xenopodimorph evolution. Zoological Journal of the Linnean Society 139:439476.
Báez, A. M., and Rage, J.-C. 1998. Pipid frogs from the Upper Cretaceous of In Beceten, Niger. Palaeontology 41:669691.
Báez, A. M., Trueb, L., and Calvo, J. O. 2000. The earliest known pipoid frog from South America: a new genus from the middle Cretaceous of Argentina. Journal of Vertebrate Paleontology 20:490500.
Berman, D. S., Reisz, R. R., and Eberth, D. A. 1985. Ecolsonia cutlerensis, an early Permian dissorophid amphibian from the Cutler Formation of north-central New Mexico. Circular of the New Mexico Bureau of Mines and Mineral Resources 191:131.
Bininda-Edmonds, O. R. P., Gittleman, J. L., and Kelly, C. K. 2001. Flippers versus feet: comparative trends in aquatic and non-aquatic carnivores. Journal of Animal Ecology 70:386400.
Bolt, J. R. 1969. Lissamphibian origins: possible protolissamphibian from the Lower Permian of Oklahoma. Science 166:888891.
Bolt, J. R. 1977. Dissorophoid relationships and ontogeny, and the origin of the Lissamphibia. Journal of Paleontology 51:235249.
Bolt, J. R. 1979. Amphibamus grandiceps as a juvenile dissorophid: evidence and implications. Pp. 529563in Nitecki, M. H., ed. Mazon Creek fossils. Academic Press, London.
Bossy, K. V. H. 1976. Morphology, paleoecology, and evolutionary relationships of the Pennsylvanian urocordylid nectrideans (subclass Lepospondyli, class Amphibia). Ph.D. dissertation. Yale University, New Haven, Conn.
Buffrénil, V. de, and Mazin, J.-M. 1990. Bone histology of the ichthyosaurs: comparative data and functional interpretation. Paleobiology 16:435447.
Buffrénil, V. de, and Mazin, J.-M. 1992. Contribution de l'histologie osseuse à l'interprétation paléobiologique du genre Placodus Agassiz, 1833 (Reptilia, Placodontia). Revue de Paléobiologie 11:397407.
Buffrénil, V. de, and Mazin, J.-M. 1993. Some aspects of skeletal growth in Triassic and post-Triassic ichthyosaurs as revealed by bone histology. Pp. 6368in Pinna, G. and Mazin, J.-M., eds. Evolution, ecology and biogeography of the Triassic reptiles. Paleontologia Lombarda della Società Italiana di Scienze Naturali e del Museo Civico di Storia Naturale di Milano, nuova serie, Milan.
Buffrénil, V. de, and Rage, J.-C. 1993. La “pachyostose” vertébrale de Simoliophis (Reptilia, Squamata): données comparatives et considérations fonctionnelles. Annales de Paléontologie 79:415–335.
Buffrénil, V. de, and Schoevaert, D. 1988. On how the periosteal bone of the delphinid humerus becomes cancellous: ontogeny of a histological specialization. Journal of Morphology 198:149164.
Buffrénil, V. de, and Schoevaert, D. 1989. Données quantitatives et observations histologiques sur la pachyostose du squelette du dugong, Dugong dugon (Müller) (Sirenia, Dugongidae). Canadian Journal of Zoology 67:21072119.
Buffrénil, V. de, Mazin, J. M., and A. de Ricqlèes. 1987. Caractères structuraux et mode de croissance du fémur d'Omphalosaurus nisseri, ichthyosaurien du Trias Moyen de Spitsberg. Annales de Paléontologie 73:195216.
Buffrénil, V. de, de Ricqlès, A., Sigogneau-Russell, D., and Buffetaut, E. 1990. L'histologie osseuse des champsosauridés: données descriptives et interprétation fonctionnelle. Annales de Paléontologie 76:255275.
Bystrow, A. P. 1944. Kotlassia prima Amalitzky. Geological Society of America Bulletin 55:379416.
Carroll, R. L. 1964. Early evolution of the dissorophid amphibians. Bulletin of the Museum of Comparative Zoology 131:161250.
Carroll, R. L. 1985. Evolutionary constraints in aquatic diapsid reptiles. Palaeontology 33:145155.
Carroll, R. L. 1988. Vertebrate paleontology and evolution. W. H. Freeman, New York.
Carroll, R. L., and Gaskill, P. 1978. The order Microsauria. American Philosophical Society, Philadelphia.
Castanet, J., and Caetano, M. H. 1995. Influence du mode de vie sur les caractéristiques pondérales et structurales du squelette chez les amphibiens anoures. Canadian Journal of Zoology 73:234242.
Castanet, J., Rogers, K. Curry, Cubo, J., and Boisard, J.-J. 2000. Periosteal bone growth rates in extant ratites (ostriche and emu): implications for assessing growth in dinosaurs. Comptes Rendus de l'Académie des Sciences de Paris, Sciences de la vie/Life Sciences 323:543550.
Castanet, J., Cubo, J., and de Margerie, E. 2001. Signification de l'histodiversité osseuse: le message de l'os. Biosystema 19:133147.
Coates, M. I., and Clack, J. A. 1991. Fish-like gills and breathing in the earliest known tetrapod. Nature 352:234236.
Dubois, A. 1992. Notes sur la classification des Ranidae (amphibiens anoures). Bulletin Mensuel de la Société Linnéenne de Lyon 61:305352.
Dubois, A., and Ohler, A. 1994. Frogs of the subgenus Pelophylax (Amphibia, Anura, genus Rana): a catalogue of available and valid scientific names, with comments on name-bearing types, complete synonymies, proposed common names, and maps showing all type localities. Zoologica Poloniae 39:139204.
Duellman, W. E., and Trueb, L. 1986. Biology of amphibians. McGraw-Hill, New York.
Estes, R. 1969. The fossil record of amphiumid salamanders. Breviora 322:111.
Fawcett, D. W. 1942. The amedullary bones of the Florida manatee (Trichechus latirostris). American Journal of Anatomy 71:271309.
Fish, F. E., and Stein, B. R. 1991. Functional correlates of differences in bone density among terrestrial and aquatic genera in the family Mustelidae (Mammalia). Zoomorphology 110:339345.
Ford, L., and Cannatella, D. C. 1993. The major clades of frogs. Herpetological Monographs 7:94117.
Gao, K.-Q., and Shubin, N. H. 2001. Late Jurassic salamanders from northern China. Nature 410:574577.
Gao, K.-Q., and Shubin, N. H. 2003. Earliest known crown-group salamanders. Nature 422:4244828.
Gao, K., and Wang, Y. 2001. Mesozoic anurans from Liaoning province, China, and phylogenetic relationships of archaeobatrachian anuran clades. Journal of Vertebrate Paleontology 21:460476.
Girondot, M., and Laurin, M. 2003. Bone profiler: a tool to quantify, model and statistically compare bone section compactness profiles. Journal of Vertebrate Paleontology 23:458461.
Golubev, V. K. 1998. Narrow-armored chroniosuchians (Amphibia, Anthracosauromorpha) from the late Permian of Eastern Europe. Paleontological Journal 32:278287.
Hay, J. M., Ruvinsky, I., Hedges, S. B., and Maxson, L. R. 1995. Phylogenetic relationships of amphibian families inferred from DNA sequences of mitochondrial 12S and 16S ribosomal RNA genes. Molecular Biology and Evolution 12:928937.
Henrici, A. C., and Báez, A. M. 2001. First occurrence of Xenopus (Anura: Pipidae) on the Arabian peninsula: a new species from the upper Oligocene of Yemen. Journal of Paleontology 75:870882.
Hua, S., and de Buffrénil, V. 1996. Bone histology as a clue in the interpretation of functional adaptations in the Thalattosuchia (Reptilia, Crocodylia). Journal of Vertebrate Paleontology 16:703717.
Ivakhnenko, M. F., Golubev, V. K., Gubin, Y. M., Kalandadze, N. N., Novikov, I. V., Sennikov, A. G., and Rautian, A. S. 1997. Permian and Triassic tetrapods of Eastern Europe. Geos, Moscow.
Janvier, P. 1996. Early vertebrates. Clarendon, Oxford.
Larson, A., and Dimmick, W. W. 1993. Phylogenetic relationships of the salamander families: an analysis of congruence among morphological and molecular characters. Herpetological Monographs 7:7793.
Laurin, M. 1998. The importance of global parsimony and historical bias in understanding tetrapod evolution, Part I. Systematics, middle ear evolution, and jaw suspension. Annales des Sciences Naturelles, Zoologie et Biologie Animale, 13e série, 19:142.
Laurin, M. 2004. The evolution of body size, Cope's rule and the origin of amniotes. Systematic Biology 53:594622.
Laurin, M., and Reisz, R. R. 1995. A reevaluation of early amniote phylogeny. Zoological Journal of the Linnean Society 113:165223.
Leclair, R. Jr., Lamontagne, C., and Aubin, A. 1993. Allométrie de la masse du squelette chez des amphibiens anoures. Canadian Journal of Zoology 71:352357.
Legendre, P., Lapointe, F.-J., and Casgrain, P. 1994. Modeling brain evolution from behavior: a permutational regression approach. Evolution 48:14871499.
Lehman, J.-P. 1955. Rachitomi. Pp. 67125in Piveteau, J., ed. Traité de Paléontologie. Masson, Paris.
Madar, S. I. 1998. Structural adaptations of early archaeocete long bones. Pp. 353378in Thewissen, J. G. M., ed. The emergence of whales—evolutionary patterns in the origin of Cetacea. Plenum, New York.
Maddison, W. P. 1990. A method for testing the correlated evolution of two binary characters: are gains or losses concentrated on certain branches of a phylogenetic tree? Evolution 44:539557.
Maddison, W. P. 1991. Squared-change parsimony reconstructions of ancestral states for continuous-valued characters on a phylogenetic tree. Systematic Zoology 40:304314.
Maddison, W. P., and Maddison, D. R. 2002. Mesquite: a modular system for evolutionary analysis, Version 0.992.
Maddison, W. P., Maddison, D. R., and Midford, P. 2002. Tree-Farm package of modules for Mesquite, Version 0.992.
Martin, R. F. 1972. Evidence from osteology. Pp. 3770in Blair, W. F., ed. Evolution in the genus Bufo. University of Texas Press, Austin.
Milner, A. C. 1980. A review of the Nectridea (Amphibia). Pp. 377405in Panchen, A. L., ed. The terrestrial environment and the origin of land vertebrates. Academic Press, London.
Nopsca, F. B. 1923. Vorläufige Notiz über die Pachyostose und Osteosklerose einiger mariner Wirbeltiere. Anatomischer Anzeiger 56:353359.
Olson, E. C. 1967. Early Permian vertebrates. Oklahoma Geological Survey Circular 74.
Padian, K., de Ricqlès, A., and Horner, J. R. 2001. Dinosaurian growth rates and bird origins. Nature 412:405408.
Purvis, A., and Rambaut, A. 1995. Comparative analysis by independent contrasts (CAIC): an Apple Macintosh application for analysing comparative data. Cabios 11:247251.
Rambaut, A., and Charleston, M. 2001. TreeEdit. University of Oxford. Available at
de Ricqlès, A. 1974a. Recherches paléohistologiques sur les os longs des tétrapodes. V. Cotylosaures et mésosaures. Annales de Paléontologie 60:171216.
de Ricqlès, A. 1974b. Recherches paléohistologiques sur les os longs des tétrapodes. IV. Eothériodontes et pélycosaures. Annales de Paléontologie 60:139.
de Ricqlès, A. 1975a. Quelques remarques paléo-histologiques sur le problème de la néoténie chez les stégocéphales. Problémes Actuels de Paléontologie: Evolution des Vertébrés. Colloque International du Centre National de Recherche Scientifique 218:351363.
Ricqlès, A. de. 1975b. Recherches paléohistologiques sur les os longs des tétrapodes. VII. Sur la classification, la signification fonctionnelle et l'histoire des tissus oseux des tétrapodes. Première partie. Annales de Paléontologie 61:51129.
Ricqlès, A. de. 1976. Recherches paléohistologiques sur les os longs des tétrapodes. VII. Sur la classification, la signification fonctionnelle et l'histoire des tissus oseux des tétrapodes. Deuxième partie. Annales de Paléontologie 62:71126.
Ricqlès, A. de. 1977. Recherches paléohistologiques sur les os longs des tétrapodes. VII. Sur la classification, la signification fonctionnelle et l'histoire des tissus osseux des tétrapodes. Deuxième partie, suite. Annales de Paléontologie 63:3356.
Ricqlès, A. de. 1981. Recherches paléohistologiques sur les os longs des tétrapodes. VI. Stégocéphales. Annales de Paléontologie 67:141160.
Ricqlès, A. de. 1989. Les mécanismes hétérochroniques dans le retour des tétrapodes au milieu aquatique. Geobios Mémoire Spécial 12:337348.
Ricqlès, A. de. 1993. Some remarks on palaeothistology from a comparative evolutionary point of view. Pp. 3777in Grupe, G. and Garland, A. N., eds. Histology of ancient human bone. Springer, Berlin.
Ricqlès, A. de, and de Buffrénil, V. 2001. Bone histology, heterochronies and the return of tetrapods to life in water: were are we? Pp. 289310in Mazin, J. M. and de Buffrénil, V., eds. Secondary adaptation of tetrapods to life in water. Pfeil, Munich.
Romer, A. S. 1957. Origin of the amniote egg. Scientific Monthly 85:5763.
Romer, A. S. 1958. Tetrapod limbs and early tetrapod life. Evolution 12:365369.
Romer, A. S. 1966. Vertebrate paleontology. University of Chicago Press, Chicago.
Ruta, M., Coates, M. I., and Quicke, D. D. L. 2003. Early tetrapod relationships revisited. Biological Reviews 78:251345.
Skulan, J. 2000. Has the importance of the amniote egg been overstated? Zoological Journal of the Linnean Society 130:235261.
Sullivan, C., and Reisz, R. R. 1999. First record of Seymouria (Ver-tebrata: Seymouriamorpha) from Early Permian fissure fills at Richards Spur, Oklahoma. Canadian Journal of Earth Sciences 36:12571266.
Sumida, M., Ogata, M., and Nishioka, M. 2000. Molecular phylogenetic relationships of pond frogs distributed in the palearctic region inferred from DNA sequences of mitochondrial 12S ribosomal RNA and cytochrome b genes. Molecular Phylogenetics and Evolution 16:278285.
Sumida, S. S. 1997. Locomotor features of taxa spanning the origin of amniotes. Pp. 353398in Sumida, S. and Martin, K., eds. Amniote origins: completing the transition to land. Academic Press, London.
Sumida, S. S., Berman, D. S., and Martens, T. 1998. A new trematopid amphibian from the Lower Permian of central Germany. Palaeontology 41:605629.
Swofford, D. L., and Maddison, W. P. 1987. Reconstructing ancestral character states under Wagner parsimony. Mathematical Biosciences 87:199229.
Taylor, M. A. 1994. Stone, bone or blubber? Buoyancy control strategies in aquatic tetrapods. Pp. 151161in Maddock, L., Bone, Q., and Rayner, J. M. V., eds. Mechanics and physiology of animals swimming. Cambridge University Press, Cambridge.
Titus, T. A., and Larson, A. 1995. A molecular phylogenetic perspective on the evolutionary radiation of the salamander family Salamandridae. Systematic Biology 44:125151.
Titus, T. A., and Larson, A. 1996. Molecular phylogenetics of desmognathine salamanders (Caudata: Plethodontidae): a reevaluation of evolution in ecology, life history and morphology. Systematic Biology 45:451472.
Trueb, L. 1999. The early Cretaceous pipoid anuran, Thoraciliacus: redescription, revaluation, and taxonomic status. Herpetologica 55:139157.
Uzzell, T. 1982. Immunological relationship of Western Palearctic Water Frogs (Salientia: Ranidae). Amphibia-Reptilia 3:135143.
Veith, M., Steinfartz, S., Zardoya, R., Seithz, A., and Meyer, A. 1998. A molecular phylogeny of “true” salamanders (family Salamandridae) and the evolution of terrestriality of reproductive modes. Journal of Zoological Systematics and Evolutionary Research 36:716.
Wall, W. P. 1983. The correlation between high limb-bone density and aquatic habits in recent mammals. Journal of Paleontology 57:197207.
Watson, D. M. S. 1914. Procolophon trigoniceps, a cotylosaurian reptile from South Africa. Proceedings of the Zoological Society of London 2022:735747.
Wellstead, C. F. 1991. Taxonomic revision of the Lysorophia, Per-mo-Carboniferous lepospondyl amphibians. Bulletin of the American Museum of Natural History 209:190.
Werneburg, R. 1991. Die Branchiosaurier aus dem Unterrotliegend des Döhlener Beckens bei Dresden. Veröffentlichungen des Naturhistorisches Museum Schleusingen 6:7599.
Wiffen, J., de Buffrénil, V., de Ricqlès, A., and Mazin, J.-M. 1995. Ontogenetic evolution of bone structure in late Cretaceous Plesiosauria from New Zealand. Geobios 28:625640.
Williston, S. W. 1911. A new family of reptiles from the Permian of New Mexico. American Journal of Science 31:378398.
Witmer, L. M. 1995. The extant phylogenetic bracket and the importance of reconstructing soft tissues in fossils. Pp. 1933in Thomason, J. J., ed. Functional morphology in vertebrate paleontology. Cambridge University Press, New York.
Yamaoka, K., Nakagawa, T., and Uno, T. 1978. Application of Akaike's information criterion (AIC) in the evaluation of linear pharmacokinetic equations. Journal of Pharmacokinetics and Biopharmaceutics 6:165175.


Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed