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Bone histology of Azendohsaurus laaroussii: Implications for the evolution of thermometabolism in Archosauromorpha

  • Jorge Cubo (a1) and Nour-Eddine Jalil (a2)


This paper is aimed at constraining the phylogenetic frame of the acquisition of endothermy by Archosauromorpha. We analyzed the bone histology of Azendohsaurus laaroussii. Stylopodial and zeugopodial bones show three tissue types: (1) avascular lamellar zonal bone formed at low growth rates; (2) a scaffold of parallel-fibered bone containing either small primary osteons or simple vascular canals; and (3) fibrolamellar bone formed at high growth rates. We used quantitative histology to infer the thermometabolic regime of this taxon. We define endothermy as the presence of any mechanism of nonshivering thermogenesis that increases both body temperature and resting metabolic rate. Thus, estimating the resting metabolic rate of an extinct organism may be a good proxy to infer its thermometabolic regime (endothermy vs. ectothermy). High resting metabolic rates have been shown to be primitive for the clade Prolacerta–Archosauriformes. Therefore, we inferred the resting metabolic rates of A. laaroussii, a sister group of this clade, and of 14 extinct related taxa, using phylogenetic eigenvector maps. All the inferences obtained are included in the range of variation of resting metabolic rates measured in mammals and birds, so we can reasonably assume that all these taxa (including Azendohsaurus) were endotherms. A parsimony optimization of the presence of endothermy on a phylogenetic tree of tetrapods shows that this derived character state was acquired by the last common ancestor of the clade Azendohsaurus–Archosauriformes and that there is a reversion in Crocodylia.



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Bernard, A., Lécuyer, C., Vincent, P., Amiot, R., Bardet, N., , N., Buffetaut, E., Cuny, G., Fourel, F., Martineau, F., Mazin, J. M., and Prieur, A.. 2010. Regulation of body temperature by some Mesozoic marine reptiles. Science 328:13791382.
Bonaparte, J. F. 1976. Pisanosaurus mertii Casamiquela and the origin of the Ornithischia. Journal of Paleontology 50:808820.
Botha-Brink, J., and Smith, R. M. H.. 2011. Osteohistology of the Triassic Archosauromorphs Prolacerta, Proterosuchus, Euparkeria, and Erythrosuchus from the Karoo Basin of South Africa. Journal of Vertebrate Paleontology 31:12381254.
Buffrenil, V. de, and Mazin, J .M. 1990. Bone histology of the ichthyosaurs: comparative data and functional interpretation. Paleobiology 16:435447.
Cubo, J., Le Roy, N., Martinez-Maza, C., and Montes, L.. 2012. Paleohistological estimation of bone growth rate in extinct archosaurs. Paleobiology 38:335349.
Cubo, J., Woodward, H., Wolff, E., and Horner, J. R.. 2015. First reported cases of biomechanically adaptive bone modeling in non-avian dinosaurs. PLoS ONE 10:e0131131.
Cubo, J., Hui, M., Clarac, F., and Quilhac, A.. 2017. Static osteogenesis does not precede dynamic osteogenesis in periosteal ossification of Pleurodeles (Caudata, Amphibia) and Pogona (Squamata, Lepidosauria). Journal of Morphology 278:621628.
Davesne, D., Meunier, F. J., Friedman, M., Benson, R. B. J., and Otero, O. 2018. Histology of the endothermic opah (Lampris sp.) suggests a new structure–function relationship in teleost fish bone. Biology Letters 14:20180270. doi: 10.1098/rsbl.2018.0270.
Dutuit, J.-M. 1972. Découverte d'un Dinosaure ornithischien dans le Trias supérieur de l'Atlas occidental marocain. Comptes Rendus de l'Académie des Sciences, Paris 275:28412844.
Dutuit, J.-M. 1976. Introduction à l’étude paléontologique du Trias continental marocain. Description des premiers Stégocéphales recueillis dans le Couloir d'Argana (Atlas occidental). Mémoires du Muséum National d'Histoire Naturelle, nouvelle série C 36:1253.
Ezcurra, M. D. 2016. The phylogenetic relationships of basal archosauromorphs, with an emphasis on the systematics of proterosuchian archosauriforms. PeerJ 4:e1778.
Ezcurra, M. D., Scheyer, T. M., and Butler, R. J.. 2014. The origin and early evolution of Sauria: Reassessing the Permian saurian fossil record and the timing of the crocodile-lizard divergence. PLoS ONE 9:e89165.
Ferretti, A., Palumbo, C., Contri, M., and Marotti, G.. 2002. Static and dynamic osteogenesis: two different types of bone formation. Anatomy and Embryology 206:2129.
Fleischle, C. V., Wintrich, T., and Sander, P. M. 2018. Quantitative histological models suggest endothermy in plesiosaurs. PeerJ 6:25. doi: 10.7717/peerj.4955.
Flynn, J. J., Parrish, J. M., Rakotosamimanana, B., Simpson, W. F., Whatley, R. B., and Wyss, A. R.. 1999. A Triassic fauna from Madagascar, including early dinosaurs. Science 286:763765.
Flynn, J. J., Nesbitt, S. J., Parrish, J. M., Ranivoharimana, R., and Wyss, A. R.. 2010. A new species of Azendohsaurus (Diapsida: Archosauromorpha) from the Triassic Isalo Group of southestern Madagascar: cranium and mandible. Palaeontology 53:669688.
Francillon-Vieillot, H., de Buffrénil, V., Castanet, J., Geraudie, J., Meunier, F., Sire, J. Y., Zylberberg, L., and de Ricqlès, A.. 1990. Microstructure and mineralization of vertebrate skeletal tissues. Pp. 471548 in Carter, J. G., ed. Skeletal biomineralization: patterns, processes and evolutionary trends. Van Nostrand Reinhold, New York.
Galton, P. M. 1985. Diet of Prosauropod dinosaurs from the Late Triassic and Early Jurassic. Lethaia 18:105123.
Galton, P. M. 1990. Basal Sauropodomorpha–Prosauropoda. Pp. 320344 in Weishampel, D. B., Dodson, P., and Osmólska, H., eds. The Dinosauria. University of California Press, Berkeley.
Gauffre, F.-X. 1993. The prosauropod dinosaur Azendohsaurus laaroussii from the Upper Triassic of Morocco. Palaeontology 36:897908.
Grafen, A. 1989. The phylogenetic regression. Philosophical Transactions of the Royal Society of London B 326:119157.
Guenard, G., Legendre, P., and Peres-Neto, P.. 2013. Phylogenetic eigenvector maps: a framework to model and predict species traits. Methods in Ecology and Evolution 4:11201131.
Houssaye, A., Lindgren, J., Pellegrini, R., Lee, A. H., Germain, D., and Polcyn, M. J.. 2013. Microanatomical and histological features in the long bones of mosasaurine mosasaurs (Reptilia, Squamata)—implications for aquatic adaptation and growth rates. PLoS ONE 8(10):112. doi: 10.1371/journal.pone.0076741.
Hunt, A. P., and Lucas, S. P.. 1994. Ornithischian dinosaurs from the Upper Triassic of the United States. Pp. 227241 in Fraser, N. C. and Sues, H.-D., eds. In the shadow of the dinosaurs. Early Mesozoic tetrapods. Cambridge University Press, Cambridge.
Jalil, N. E., and Knoll, F.. 2002. Is Azendohsaurus laaroussii (Carnian Morocco) a dinosaur? Journal of Vertebrate Paleontology 22(Suppl. to No. 3):70A.
Jaquier, V. P., and Scheyer, T. M.. 2017. Bone histology of the Middle Triassic long-necked reptiles Tanystropheus and Macrocnemus (archosauromorpha, Protorosauria). Journal of Vertebrate Paleontology 37:e1296456.
Khaldoun, F. 2014. Les vertébrés du Permien et du Trias du Maroc (Bassin d'Argana, Haut Atlas Occidental) avec la réévaluation d’Azendohsaurus laaroussii (Reptilia, Archosauromorpha) et la description de Reptilia Moradisaurinae et Rhynchosauria nouveaux: anatomie, relations phylogénétiques et implications biostratigraphiques. Unpublished Ph.D. thesis. University Cadi Ayyad, Marrakesh, Morocco. 342 pp.
Lamm, E. T. 2013. Preparation and sectioning of specimens. Pp. 55160 in Bone histology of fossil tetrapods: advancing methods, analysis, and interpretation. University of California Press, Berkeley.
Legendre, L. J., Segalen, L., and Cubo, J.. 2013. Evidence for high bone growth rate in Euparkeria obtained using a new paleohistological inference model for the humerus. Journal of Vertebrate Paleontology 33:13431350.
Legendre, L. J., Guenard, G., Botha-Brink, J., and Cubo, J.. 2016. Palaeohistological evidence for ancestral high metabolic rate in Archosaurs. Systematic Biology 65:989996.
Lowell, B. B., and Spiegelman, B. M.. 2000. Towards a molecular understanding of adaptive thermogenesis. Nature 404:652660.
Maddison, W. P., and Maddison, D. R.. 2015. Mesquite: a modular system for evolutionary analysis.
Marotti, G. 2010. Static and dynamic osteogenesis. Italian Journal of Anatomy and Embryology/Archivio italiano di anatomia ed embriologia 115:123126.
Montes, L., Le Roy, N., Perret, M., De Buffrenil, 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 92:6376.
Mukherjee, D. 2015. New insights from bone microanatomy of the Late Triassic Hyperodapedon (Archosauromorpha, Rhynchosauria): implications for archosauromorph growth strategy. Palaeontology 58:313339.
Nesbitt, S. 2007. The anatomy of Effigia okeeffeae (Archosauria, Suchia), theropod-like convergence, and the distribution of related taxa. Bulletin of the American Museum of Natural History 302:184.
Nesbitt, S. J., Stocker, M. R., Small, B. J., and Downs, A.. 2009. The osteology and relationships of Vancleavea campi (Reptilia: Archosauriformes). Zoological Journal of the Linnean Society 157:814864.
Nesbitt, S. J., Flynn, J. J., Pritchard, A. C., Parrish, J. M., Ranivoharimanana, L., and Wyss, A. R.. 2015. Postcranial osteology of Azendohsaurus madagaskarensis (?middle to Upper Triassic, Isalo Group, Madagascar) and its systematic position among stem archosaur reptiles. Bulletin of the American Museum of Natural History 398:1126.
Nowack, J., Giroud, S., Arnold, W., and Ruf, T.. 2017. Muscle non-shivering thermogenesis and its role in the evolution of endothermy. Frontiers in Physiology 8:ar889.
Orme, D., Freckleton, R., Thomas, G., Petzoldt, T., Fritz, S., Isaac, N., and Pearse, W.. 2013. Caper: comparative analyses of phylogenetics and evolution in R.
Padian, K., and Horner, J. R.. 2002. Typology versus transformation in the origin of birds. Trends in Ecology and Evolution 17:120124.
Padian, K., Horner, J. R., and De Ricqles, A.. 2004. Growth in small dinosaurs and pterosaurs: the evolution of archosaurian growth strategies. Journal of Vertebrate Paleontology 24:555571.
Palumbo, C., Ferretti, M., and Marotti, G.. 2004. Osteocyte dendrogenesis in static and dynamic bone formation: an ultrastructural study. Anatomical Record A 278A:474480.
Pritchard, A. C., Turner, A. H., Nesbitt, S. J., Irmis, R. B., and Smith, N. D.. 2015. Late Triassic tanystropheids (Reptilia, Archosauromorpha) from northern New Mexico (Petrified Forest Member, Chinle Formation) and the biogeography, functional morphology, and evolution of Tanystropheidae. Journal of Vertebrate Paleontology 35:e911186.
Prondvai, E., Stein, K. H. W., de Ricqles, A., and Cubo, J.. 2014. Development-based revision of bone tissue classification: the importance of semantics for science. Biological Journal of the Linnean Society 112:799816.
R Core Team. 2016. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
Ricqlès, A. de, Padian, K., Horner, J. R., and Francillon-Vieillot, H.. 2000. Palaeohistology of the bones of pterosaurs (Reptilia: Archosauria): anatomy, ontogeny, and biomechanical implications. Zoological Journal of the Linnean Society 129:349385.
Ricqlès, A. de, Padian, K., and Horner, J. R.. 2003. On the bone histology of some Triassic pseudosuchian archosaurs and related taxa. Annales de Paléontologie 89:67101.
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. Annales de Paléontologie 94:5776.
Rowland, L. A., Bal, N. C., and Periasamy, M.. 2015. The role of skeletal-muscle-based thermogenic mechanisms in vertebrate endothermy. Biological Reviews 90:12791297.
Stein, K., and Prondvai, E.. 2014. Rethinking the nature of fibrolamellar bone: an integrative biological revision of sauropod plexiform bone formation. Biological Reviews 89:2447.
Thulborn, R. A. 1973. Teeth of ornithischian dinosaurs from the Upper Jurassic of Portugal. Serviços Geológicos de Portugal, Memoria 22: 89134.
Thulborn, R. A. 1974. A new heterodontosaurid dinosaur (Reptilia: Ornithischia) from the Upper Triassic Red Beds of Lesotho. Zoological Journal of the Linnean Society of London 55:151175.
Tumarkin-Deratzian, A. R. 2007. Fibrolamellar bone in wild adult Alligator mississippiensis. Journal of Herpetology 41:341345.
Veiga, F. H., Soares, M. B., and Sayao, J. M.. 2015. Osteohistology of hyperodapedontine rhynchosaurs from the Upper Triassic of Southern Brazil. Acta Palaeontologica Polonica 60:829836.
Weishampel, D. B. 1990. Dinosaurian distribution. Pp. 63139 in Weishampel, D. B., Dodson, P., and Osmólska, H., eds. The Dinosauria. University of California Press, Berkeley.
Werning, S., and Irmis, R. B.. 2011. Reconstructing growth of the basal archosauromorph Trilophosaurus. Integrative and Comparative Biology 51:E147.
Werning, S., and Nesbitt, S. J.. 2016. Bone histology and growth in Stenaulorhynchus stockleyi (Archosauromorpha: Rhynchosauria) from the Middle Triassic of the Ruhuhu Basin of Tanzania. Comptes Rendus Palevol 15:163175.

Bone histology of Azendohsaurus laaroussii: Implications for the evolution of thermometabolism in Archosauromorpha

  • Jorge Cubo (a1) and Nour-Eddine Jalil (a2)


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