Hostname: page-component-cd9895bd7-8ctnn Total loading time: 0 Render date: 2024-12-27T10:26:12.541Z Has data issue: false hasContentIssue false
  • English
  • Français

Paleohistological estimation of bone growth rate in extinct archosaurs

Published online by Cambridge University Press:  08 April 2016

Jorge Cubo ,
Nathalie Le Roy ,
Cayetana Martinez-Maza  and
Laetitia Montes
Jorge Cubo*
Affiliation:
UPMC, Université Paris 06, UMR 7193, ISTeP; and CNRS, UMR 7193, ISTeP, 4 place Jussieu, BC 19, F-75005, Paris, France. E-mail: jorge.cubo_garcia@upmc.fr
Nathalie Le Roy
Affiliation:
CNRS, UMR 5561, Biogéosciences, Université de Bourgogne 6, boulevard Gabriel, Dijon 21000, France
Cayetana Martinez-Maza
Affiliation:
UPMC, Université Paris 06, UMR 7193, ISTeP; and CNRS, UMR 7193, ISTeP, 4 place Jussieu, BC 19, F-75005, Paris, France
Laetitia Montes
Affiliation:
UPMC, Université Paris 06, UMR 7193, ISTeP; and CNRS, UMR 7193, ISTeP, 4 place Jussieu, BC 19, F-75005, Paris, France
*
∗Corresponding author
Get access Rights & Permissions [Opens in a new window]

Abstract

The clade Archosauria contains two very different sister groups in terms of diversity (number of species) and disparity (phenotypic variation): Crurotarsi (taxa more closely related to crocodiles than to birds) and Ornithodira (pterosaurs and dinosaurs including birds). The extant species of Crurotarsi may constitute a biased sample of past biodiversity regarding growth patterns and metabolic rates. Bone histological characters can be conserved over hundreds of millions of years in the fossil record and potentially contain information about individual age at death, age at sexual maturity, bone growth rates, and basal metabolic rates of extinct vertebrates. Using a sample of extant amniotes, we have constructed a paleobiological model to estimate bone growth rate from bone histological traits. Cross-validation tests show that this model is reliable. We then used it to estimate bone growth rates in a sample of extinct archosaurs including Crurotarsi and Ornithodira. After testing for phylogenetic signal, optimization of femoral growth rates through squared change parsimony onto a time-calibrated tree of amniotes shows two divergent evolutionary trends: whereas bone growth rates increase from the last common ancestor of Ornithodira to extant birds, they decrease from the last common ancestor of Crurotarsi to extant crocodiles. However, we conclude, on the basis of recent evidence for unidirectional airflow in the lungs of alligators, that crocodiles may have retained the capacity of growing at high rates.

Type
Articles
Information
Paleobiology , Volume 38 , Issue 2 , Spring 2012 , pp. 335 - 349
Copyright
Copyright © The Paleontological Society 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Literature Cited

Amprino, R. 1947. La structure du tissu osseux envisagée comme expression de différences dans la vitesse de l'accroissement. Archives of Biology 58:315–330.Google Scholar
Boef, M. de, and Larsson, H. C. E. 2007. Bone microstructure: quantifying bone vascular orientation. Canadian Journal of Zoology 85:63–70.Google Scholar
Bourdon, E., de Ricqlès, A., and Cubo, J. 2009. A new Transantarctic relationship: morphological evidence for a Rheidae–Dromaiidae–Casuariidae clade (Aves, Palaeognathae, Ratitae). Zoological Journal of the Linnean Society 156:641–663.Google Scholar
Bybee, P. J., Lee, A. H., and Lamm, E. T. 2006. Sizing the Jurassic theropod dinosaur Allosaurus: assessing growth strategy and evolution of ontogenetic scaling of limbs. Journal of Morphology 267:347–359.Google Scholar
Caldwell, M. W. 1999. Squamate phylogeny and the relationship of snakes and mosasauroids. Zoological Journal of the Linnean Society 125:115–147.Google Scholar
Case, T. J. 1978. Speculations on the growth rate and reproduction of some dinosaurs. Paleobiology 4:320–326.Google Scholar
Castanet, J., Grandin, A., Abourachid, A., and de Ricqlès, A. 1996. Expression de la dynamique de croissance dans la structure de l'os périostique chez Anas platyrhynchos. Comptes Rendus de l'Académie des Sciences, Paris, série 3, Sciences de la Vie 319:301–308.Google Scholar
Castanet, J., Curry Rogers, K., 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, Paris, série 3, Sciences de la Vie 323:543–550.Google ScholarPubMed
Chatterjee, S. 2002. The morphology and systematics of Polarornis, a cretaceous loon (Aves: Gaviidae) from Antarctica. Pp. 125–155inZhou, Z.and Zhang, F., eds. Proceedings of the 5th Symposium of the Society of Avian Paleontology and Evolution, Beijing, 1–4 June 2000. Science Press, Beijing.Google Scholar
Claessens, L. P. A. M., O'Connor, P. M., and Unwin, D. M. 2009. Respiratory evolution facilitated the origin of Pterosaur flight and aerial gigantism. PLoS ONE 4(2):e4497, 1–8.Google Scholar
Clarke, J. A., Tambussi, C. P., Noriega, J. I., Erickson, G. M., and Ketcham, R. A. 2005. Definitive fossil evidence for the extant avian radiation in the Cretaceous. Nature 433:305–308.Google Scholar
Cooper, L. N., Lee, A. H., Taper, M. L., and Horner, J. R. 2008. Relative growth rates of predator and prey dinosaurs reflect effects of predation. Proceedings of the Royal Society of London B 275:2609–2615.Google Scholar
Cubo, J., and Manosa, S. 1999. Evidence for heterochrony in the evolution of the goshawk Accipiter gentilis (Accipitridae, Aves). Annales des Sciences Naturelles, Zoologie 20:67–72.Google Scholar
Cubo, J., Fouces, V., Gonzalez-Martin, M., Pedrocci, V., and Ruiz, X. 2000. Nonheterochronic developmental changes underlie morphological heterochrony in the evolution of Ardeidae. Journal of Evolutionary Biology 13:269–276.Google Scholar
Cubo, J., Azagra, D., Casinos, A., and Castanet, J. 2002. Heterochronic detection through a function for the ontogenetic variation of bone shape. Journal of Theoretical Biology 215:57–66.Google Scholar
Cubo, J., Legendre, P., de Ricqlès, A., Montes, L., de Margerie, E., Castanet, J., and Desdevises, Y. 2008. Phylogenetic, functional, and structural components of variation in bone growth rate of amniotes. Evolution and Development 10:217–227.Google Scholar
Cubo, J., Ponton, F., Laurin, M., de Margerie, E., and Castanet, J. 2005. Phylogenetic signal in bone microstructure of sauropsids. Systematic Biology 54:562–574.Google Scholar
Curry, K. A. 1999. Ontogenetic histology of Apatosaurus (Dinosauria: Sauropoda): new insights on growth rates and longevity. Journal of Vertebrate Paleontology 19:654–665.Google Scholar
Desdevises, Y., Legendre, P., Azouzi, L., and Morand, S. 2003. Quantifying phylogenetically structured environmental variation. Evolution 57:2647–2652.Google Scholar
Diniz-Filho, J. A. F., de Sant' Ana, C. E. R., and Bini, L. M. 1998. An eigenvector method for estimating phylogenetic inertia. Evolution 52:1247–1262.Google Scholar
Erickson, G. M. 2005. Assessing dinosaur growth patterns: a microscopic revolution. Trends in Ecology and Evolution 20:677–684.Google Scholar
Erickson, G. M., and Brochu, C. A. 1999. How the ‘terror crocodile’ grew so big. Nature 398:205–206.Google Scholar
Erickson, G. M., Curry Rogers, K., Varricchio, D. J., Norell, M. A., and Xu, X. 2007. Growth patterns in brooding dinosaurs reveals the timing of sexual maturity in non-avian dinosaurs and genesis of the avian condition. Biology Letters 3:558–561.CrossRefGoogle ScholarPubMed
Estes, R. 1982. The fossil record and early distribution of lizards. Pp. 365–398inAdvances in herpetology and evolutionary biology: essays in honor of E. E. Williams. Harvard University Press, Cambridge.Google Scholar
Estes, R., de Queiroz, K., and Gauthier, J. 1988. Phylogenetic relationships within Squamata. Pp. 119–281inEstes, R.and Pregill, G., eds. Phylogenetic relationships of the lizard families. Stanford University Press, Stanford, Calif.Google Scholar
Evans, S. E. 2003. At the feet of the dinosaurs: the early history and radiation of lizards. Biological Reviews 78:513–551.Google Scholar
Farmer, C. G., and Sanders, K. 2010. Unidirectional airflow in the lungs of alligators. Science 327:338–340.CrossRefGoogle ScholarPubMed
Felsenstein, J. 1985. Phylogenies and the comparative method. American Naturalist 125:1–15.Google Scholar
Gaffney, E. S., and Meylan, P. A. 1988. A phylogeny of turtles. Pp. 157–219inBenton, M. J., ed. The phylogeny and classification of tetrapods. Clarendon, Oxford.Google Scholar
Hope, S. 2002. The Mesozoic radiation of Neornithes. Pp. 339–388inChiappe, L. M.and Witmer, L. M., eds. Mesozoic birds: above the heads of dinosaurs. University of California Press, Berkeley.Google Scholar
Horner, J. R., de Ricqlès, A., and Padian, K. 1999. Variation in dinosaur skeletochronology indicators: implications for age assessment and physiology. Paleobiology 25:295–304.CrossRefGoogle Scholar
Horner, J. R., de Ricqlès, A., and Padian, K. 2000. Long bone histology of the hadrosaurid dinosaur Maiasaura peeblesorum: growth dynamics and physiology based on an ontogenetic series of skeletal elements. Journal of Vertebrate Paleontology 20:115–129.CrossRefGoogle Scholar
Horner, J. R., de Ricqlès, A., and Padian, K. 2001. Comparative osteohistology of some embryonic and perinatal archosaurs: phylogenetic and behavioral implications for dinosaurs. Paleobiology 27:39–58.Google Scholar
Kirkwood, J. K., Duignan, P. J., Kember, N. F., Bennett, P. M., and Price, D. J. 1989. The growth rate of the tarsometatarsus bone in birds. Journal of Zoology 217:403–416.Google Scholar
Langer, M. C., Ezcurra, M. D., Bittencourt, J. S., and Novas, F. E. 2010. The origin and early evolution of dinosaurs. Biological Reviews 85:55–110.Google Scholar
Laurin, M. 2004. The evolution of body size, Cope's rule and the origin of amniotes. Systematic Biology 53:594–622.Google Scholar
Laurin, M., and Reisz, R. R. 1995. A revaluation of early amniote phylogeny. Zoological Journal of the Linnean Society 113:165–223.Google Scholar
Laurin, M., Girondot, M., and Loth, M. M. 2004. The evolution of long bone microanatomy and lifestyle in lissamphibians. Paleobiology 30:589–613.Google Scholar
Lee, A. H. 2004. Histological organization and its relationship to function in the femur of Alligator mississippiensis.. Journal of Anatomy 204:197–207.Google Scholar
Lee, A. H., and Werning, S. 2008. Sexual maturity in growing dinosaurs does not fit reptilian growth models. Proceedings of the National Academy of Sciences USA 105:582–587.Google Scholar
Lee, M. S. Y. 2001. Molecules, morphology, and the monophyly of diapsid reptiles. Contributions to Zoology 70:1–22.Google Scholar
Legendre, P., Lapointe, F. J., and Casgrain, P. 1994. Modeling brain evolution from behavior: A permutational regression approach. Evolution 48:1487–1499.Google Scholar
Maddison, W. P., and Maddison, D. R. 2009. Mesquite: a modular system for evolutionary analysis, Version 2.71 (http://mesquiteproject.org).Google Scholar
Margerie, E. de. 2002. Laminar bone as an adaptation to torsional loads in flapping flight. Journal of Anatomy 201:521–526.Google Scholar
Margerie, E. de., Cubo, J., and Castanet, J. 2002. Bone typology and growth rate: testing and quantifying “Amprino's rule” in the mallard (Anas platyrhynchos). Comptes Rendus Biologies 325:221–230.Google Scholar
Margerie, E. de., Robin, J. P., Verrier, D., Cubo, J., Groscolas, R., and Castanet, J. 2004. Assessing a relationship between bone microstructure and growth rate; a fluorescent labeling study in the King Penguin chick (Aptenodytes patagonicus). Journal of Experimental Biology 207:869–879.Google Scholar
Margerie, E. de., Sanchez, S., Cubo, J., and Castanet, J. 2005. Torsional resistance as a principal component of the structural design of long bones: comparative multivariate evidence in birds. Anatomical Record A 282:49–66.Google Scholar
Marjanovic, D., and Laurin, M. 2007. Fossils, molecules, divergence times, and the origin of lissamphibians. Systematic Biology 56:369–388.Google Scholar
Matrajt, H., Bordier, P., Martin, J., and Hioco, D. 1967. Technique pour l'inclusion des biopsies osseuses non decalcifies. Journal of Microscopy 6:499–504.Google Scholar
Midford, P. E., Garland, T. Jr., and Maddison, W. P. 2003. PDAP package for Mesquite (http://mesquiteproject.org/pdap_mesquite/index.html).Google Scholar
Montes, L., Le Roy, N., Perret, M., de Buffrénil, V., Castanet, J., and Cubo, J. 2007. Relationships between bone growth rate, body mass and resting metabolic rate in growing amniotes: a phylogenetic approach. Biological Journal of the Linnean Society 92:63–76.Google Scholar
Müller, J., and Reisz, R. R. 2005. Four well-constrained calibration points from the vertebrate fossil record for molecular clock estimates. BioEssays 27:1069–1075.Google Scholar
O'Connor, P. M., and Claessens, L. P. A. M. 2005. Basic avian pulmonary design and flow-through ventilation in non-avian theropod dinosaurs. Nature 436:253–256.Google Scholar
Olson, S. L., and Parris, D. C. 1987. The Cretaceous birds of New Jersey. Smithsonian Contributions to Paleobiology 63:1–22.Google Scholar
Organ, C. L., Shedlock, A. M., Meade, A., Pagel, M., and Edwards, S. V. 2007. Origin of avian genome size and structure in non-avian dinosaurs. Nature 446:180–184.Google Scholar
Padian, K., and Horner, J. R. 2002. Typology versus transformation in the origin of birds. Trends in Ecology and Evolution 17(3):120–124.Google Scholar
Padian, K., de Ricqlès, A., and Horner, J. R. 2001. Dinosaurian growth rates and bird origins. Nature 412:405–408.Google Scholar
Padian, K., Horner, J. R., and de Ricqlès, A. 2004. Growth in small dinosaurs and pterosaurs: the evolution of archosaurian growth strategies. Journal of Vertebrate Paleontology 24:555–571.Google Scholar
Ponton, F., Montes, L., Castanet, J., and Cubo, J. 2007. Bone histological correlates of high frequency flapping flight and body mass in the furculae of birds: a phylogenetic approach. Biological Journal of the Linnean Society 91:729–738.Google Scholar
Pyron, R. A. 2010. A likelihood method for assessing molecular divergence time estimates and the placement of fossil calibrations. Systematic Biology 59:185–194.Google Scholar
Reisz, R. R., and Müller, J. 2004. Molecular timescales and the fossil record: a paleontological perspective. Trends in Genetics 20:237–241.Google Scholar
Ricqlès, A. de. 1978. Sur la classification, la signification fonctionnelle et l'histoire des tissues osseux des tétrapodes. Troisième partie: evolution. Annales de Paléontologie 64:85–111.Google Scholar
Ricqlès, A. de, Padian, K., and Horner, J. R. 2003. On the bone histology of some Triassic crurotarsan archosaurs and related taxa. Annales de Paléontologie 89:67–101.Google Scholar
Ricqlès, A. de, Padian, K., Knoll, F., and Horner, J. R. 2008. On the origin of high growth rates in archosaurs and their ancient relatives: Complementary histological studies on Triassic archosauriforms and the problem of a “phylogenetic signal” in bone histology. Annals of Paleontology 94:57–76.Google Scholar
Rieppel, O. 1988. The classification of Squamata. Pp. 261–293inBenton, M. J., ed. The phylogeny and classification of the tetrapods. Clarendon, Oxford.Google Scholar
Rieppel, O., and Reisz, R. R. 1999. The origin and early evolution of turtles. Annual Review of Ecology and Systematics 30:1–22.Google Scholar
Sander, P. M. 2000. Long bone histology of the Tendaguru sauropods: implications for growth and biology. Paleobiology 26:466–488.Google Scholar
Scotese, C. R. 2001. Paleomap Project (http://www.scotese.com).Google Scholar
Starck, J. M., and Chinsamy, A. 2002. Bone microstructure and developmental plasticity in birds and other dinosaurs. Journal of Morphology 254:232–246.CrossRefGoogle ScholarPubMed
Witmer, L. M. 1995. The extant phylogenetic bracket and the importance of reconstructing soft tissues in fossils. Pp. 19–33inThomason, J. J., eds. Functional morphology in vertebrate paleontology. Cambridge University Press, New York.Google Scholar
Woodward, H., and Horner, J. 2010. Osteohistological analysis of Alligator mississippiensis indicates absence of fibrolamellar bone in crocodylians and confirms determinate growth with first report of external fundamental systems: implications for tetrapod osteohistology. Seventieth anniversary meeting of the Society of Vertebrate Paleontology, Abstracts, p. 190A.Google Scholar
Zardoya, R., and Meyer, A. 2001. The evolutionary position of turtles revised. Naturwissenschaften 88:193–200.Google Scholar