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Evolution of Sirenian Pachyosteosclerosis, a Model-case for the Study of Bone Structure in Aquatic Tetrapods

Journal of Mammalian Evolution volume 17, pages 101–120 (2010)Cite this article

Abstract

Osteosclerosis, or inner bone compaction, and pachyostosis, or outer hyperplasy of bone cortices (swollen bones), are typical features of tetrapods secondarily adapted to life in water. These peculiarities are spectacularly exemplified by the ribs of extant and extinct Sirenia. Sea cows are thus the best model for studying this kind of bone structural specializations. In order to document how these features differentiated during sirenian evolution, the ribs of 15 species, from the most basal form (Pezosiren portelli) up to extant taxa, were studied, and compared to those of other mammalian species from both morphometric and histological points of view. Pachyostosis was the first of these two specializations to occur, by the middle of the Eocene, and is a basal feature of the Sirenia. However, it subsequently regressed in some taxa that do not exhibit hyperplasic rib cortices. Osteosclerosis was only incipient in P. portelli. Its full development occurred later, by the end of the Eocene. These two structural specializations of bone are variably pronounced in extinct and extant sirenians, and relatively independent from each other, although frequently associated. They are possibly due to similar heterochronic mechanisms bearing on the timing of osteoblast activity. These results are discussed with respect to the functional constraints of locomotion in water.

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References

  • Asagiri M, Takayanagi H (2007) The molecular understanding of osteoclast differentiation. Bone 40: 251–264

    Article  CAS  PubMed  Google Scholar 

  • Bénichou OD, Laredo JD, de Vernejoul MC (2000) Type II autosomal dominant osteopetrosis (Albers-Schönberg disease): clinical and radiological manifestations in 42 patients. Bone 26(1): 87–93

    Google Scholar 

  • Brandt A (1852) Dissertationes de ossificationis processu. Inaugural dissertation, Dorpat.

  • Buffrénil V de, Rage J-C (1993) La “ pachyostose ” vertébrale de Simoliophis (Reptilia, Squamata) : données comparatives et considérations fonctionnelles. Ann Paléontol 79: 315–335

    Google Scholar 

  • Buffrénil V de, Ricqlès A de, Ray CE, Domning DP (1990a) Bone histology of the ribs of the archaeocetes (Mammalia: Cetacea). J Vertebr Palentol 10(4): 455–466

    Google Scholar 

  • Buffrénil V de, Ricqlès A de, Sigogneau-Russell D, Buffetaut E (1990b) L’histologie osseuse des Champsosauridés : données descriptives et interprétations fonctionnelles. Ann Paléontol 76(4): 255–275

    Google Scholar 

  • Buffrénil V de, Schoevaert D (1988) On how the delphinid humerus becomes cancellous: ontogeny of a histological specialization. J Morphol 198: 146–164

    Google Scholar 

  • Buffrénil V de, Schoevaert D (1989) Données quantitatives et observations histologiques sur la pachyostose du squelette du dugong, Dugong dugon (Müller) (Sirenia, Dugongidae). Can J Zool 67: 2107–2119

    Google Scholar 

  • Castanet J (2006) Time recording in bone microstructures of endothermic animals. CR Palevol 5: 629–636

    Article  Google Scholar 

  • Cave AJE, Aumonier FJ (1967) Observations on dugong histology. Quart J Roy Microsc Soc 87: 113–121

    CAS  Google Scholar 

  • Cubo J (2000) Process heterochronies in endochondral ossification. J Theor Biol 205: 343–353

    Article  CAS  PubMed  Google Scholar 

  • D’Anastasio R (2004) Idiopathic hyperostosis: epidemiology and phylogeny. J Paleopathol 16(3): 133–145

    Google Scholar 

  • Domning DP (1978) Sirenian evolution in the North Pacific Ocean. Univ Calif Publ Geol Sci 118: 1–176

    Google Scholar 

  • ——— (1994) A phylogenetic analysis of the Sirenia. In: Berta A, Demere TA (eds) Contributions in Marine Mammal Paleontology Honoring Frank C. Whitmore, Jr. Proc San Diego Soc Nat Hist, San Diego, pp 177–189

  • ——— (2000) The readaptation of Eocene sirenians to life in water. Hist Biol 14(1–2): 115–119

    Article  Google Scholar 

  • ——— (2001a) The earliest fully quadrupedal sirenian. Nature 413: 625–627

    Article  CAS  PubMed  Google Scholar 

  • ——— (2001b) Evolution of the Sirenia and Desmostylia. In: Mazin J-M, Buffrénil V de (eds) Secondary Adaptation of Tetrapods to Life in Water. Verlag Dr. F. Pfeil, München, pp 151–168

  • ——— (2001c) Sirenians, seagrasses, and Cenozoic ecological change in the Caribbean. In: Miller W III, Walker SE (eds) Cenozoic Palaeobiology: The Last 65 Million Years of Biotic Stasis and Change. Palaeogeogr, Palaeoclimatol, Palaeoecol 166(1–2): 27–50

  • ——— (2002) Sirenian evolution. In: Perrin WF, Wursig B, Thewissen JGM (eds) Encyclopedia of Marine Mammals. Academic Press, London, New York, pp 1083–1086

    Google Scholar 

  • Domning DP, Aguilera OA (2008) Fossil Sirenia of the west Atlantic and Caribbean region. VIII. Nanosiren garciae gen. et sp. nov. and Nanosiren sanchezi, sp. nov. J Vertebr Paleontol 28(2): 479–500

    Article  Google Scholar 

  • Domning DP, Buffrénil V. de (1991) Hydrostasis in the Sirenia : quantitative data and functional interpretations. Mar Mamm Sci 7(4): 331–368

    Google Scholar 

  • Domning DP, Myrick AC Jr (1980) Tetracycline marking and the possible layering rate of bone in the Amazonian manatee (Trichechus inunguis). In: Perrin WF, Myrick AC Jr (eds) Age Determination of Toothed Whales and Sirenians. Rep Int Whal Commn (Special Issue 3): 203–207

  • Fawcett DW (1942) The amedullary bones of the Florida manatee (Trichechus latirostris). Am J Anat 71: 27–309

    Article  Google Scholar 

  • Francillon-Vieillot H, Buffrénil V de, Castanet J, Geraudie J, Meunier FJ, Sire JY, Zylberberg L, Ricqlès A de (1990) Microstructures and mineralization of vertebrate skeletal tissues. In: Carter J (ed) Skeletal Biomineralizations: Patterns, Processes and Evolutionary Trends 1. Van Nostrand Reinhold, New York, pp 471–530

  • Gallivan GJ, Best RC, Kanwisher JW (1983) Temperature regulation in the Amazonian manatee, Trichechus inunguis. Physiol Zool 56: 255–262

    Google Scholar 

  • Gingerich PD, Domning DP, Blane CE, Uhen MD (1994) Cranial morphology of Protosiren fraasi (Mammalia, Sirenia) from the middle Eocene of Egypt: a new study using computed tomography. Mus Paleontol Univ Mich 29(2): 41–67

    Google Scholar 

  • Girondot M, Laurin M (2003) Bone profiler: a tool to quantify, model, and statistically compare bone-section compactness profiles. J Vertebr Paleontol 23(2): 458–461

    Article  Google Scholar 

  • Gray NM, Kimberly K, Madar S, Tomko L, Wolfe S (2007) Sink or swim? Bone buoyancy control in early cetaceans. Anat Rec 290(6): 638–653

    Article  Google Scholar 

  • Houssaye A, Buffrénil V de, Rage J-C, Bardet N (2008) An analysis of vertebral “pachyostosis” in Carentonosaurus mineaui (Mosasauroidea, Squamata) from the Cenomanian (early Late Cretaceous) of France, with comments on its phylogenetic and functional significance. J Vertebr Paleontol 28(3): 685–691

    Google Scholar 

  • Husar SL (1975) A review of the literature on the dugong (Dugong dugon). US Department of Interior Fish and Wildlife Service, Wildlife Research Report 4

  • Irvine AB (1983) Manatee metabolism and its influence on distribution in Florida. Biol Conserv 25: 315–334

    Article  Google Scholar 

  • Kaiser HE (1960) Untersuchungen zur vergleichenden Osteologie der fossilen und rezenten Pachyostosen. Palaeontograph A 114(5–6): 113–196

    Google Scholar 

  • ——— (1970) Das Abnorm in der Evolution. Acta Biotheor, suppl 9. E.J. Brill, Leyden.

  • Karsenty G (2007) The genetic transformation of bone biology. Genes Develop 13: 3037–3051

    Article  Google Scholar 

  • Key LL Jr, Ries WL (2002) Osteopetrosis. In: Bilezikian JP, Raisz LG, Rodan GA (eds) Principles of Bone Biology, vol. 2. Academic Press, San Diego, pp 1217–1227

    Google Scholar 

  • Kiprijanoff AV (1881–1883) Studien über die fossilen Reptilien Russlands. Mém Acad Imp Sci Saint Petersbourg 7: 1–144

    Google Scholar 

  • Klevezal GA (1996) Recording Structures of Mammals: Determination of Age and Reconstruction of Life History. Balkema, Rotterdam.

    Google Scholar 

  • Laurin M, Girondot M, Loth M-M (2004) The evolution of long bone microstructure and lifestyle in lissamphibians. Paleobiology 30(4): 589–613

    Article  Google Scholar 

  • Madar SI (2007) The postcranial skeleton of early Eocene pakicetid cetaceans. J Paleontol 81(1): 176–200

    Article  Google Scholar 

  • Marmontel M, O’Shea TJ, Kochman HI, Humphrey SR (1996) Age determination in manatees using growth-layer-counts in bone. Mar Mamm Sci 12(1): 54–88

    Article  Google Scholar 

  • Marsh H (1980) Age determination of the dugong (Dugong dugon [Müller]) in Northern Australia and its biological implications. In: Perrin WF, Myrick AC (eds) Age Determination in Toothed Whales and Sirenians. Rep Int Whal Commn (Spec Issue 3): 181–201

  • Marsh H, Spain AV, Heinsohn GE (1978) Minireview. Physiology of the dugong. Comp Biochem Physiol A61: 159–168

    Article  Google Scholar 

  • Meister W (1962) Histological structure of the long bones of penguins. Anat Rec 143: 377–386

    Article  CAS  PubMed  Google Scholar 

  • Nopcsa F von (1923) Vorläufige Notiz über die Pachyostose und Osteosklerose einiger mariner Wirbeltiere. Anat Anz 56: 353–359

    Google Scholar 

  • Nopcsa F von, Heidsieck E (1934) Über eine pachyostotische Rippe aus der Kreide Rügens. Acta Zool (Stockholm) 15: 431–455

    Google Scholar 

  • Parfitt AM (1982) The coupling of bone formation to bone resorption: a critical analysis of the concept and its relevance to the pathogenesis of osteoporosis. Metabol Bone Disease Rel Res 4: 1–6

    Article  CAS  Google Scholar 

  • Pilleri G, Biosca J, Via L 1989. The Tertiary Sirenia of Catalonia. Brain Anatomy Institute, University of Berne, Ostermundigen (Berne)

  • Popoff SN, Marks SC (1995) The heterogeneity of the osteopetroses reflects the diversity of cellular influences during skeletal development. Bone 17(5): 437–445

    Article  CAS  PubMed  Google Scholar 

  • Ricqlès A de (1975) Recherches paléohistologiques sur les os longs des tetrapods. VII.—Sur la classification, la signification fonctionnelle et l’histoire des tissus osseux des tétrapodes (première partie). Ann Paléontol (Vertébrés) 61: 51–129

  • ——— (1989) Les mécanismes hétérochroniques dans le retour des tétrapodes au milieu aquatique. Geobios, mém spéc 12: 337–348

    Google Scholar 

  • Ricqlès A de, Buffrénil V de (1995) Sur la présence de pachyostéosclérose chez la rhytine de Steller [Rhytina (Hydrodamalis) gigas], sirénien récent éteint. Ann Sci Nat, Zool (13ème série) 16: 47–53

  • ——— (2001) Bone histology, heterochronies and the return of tetrapods to life in water: where are we? In: Mazin J-M, Buffrénil V de (eds) Secondary Adaptation of Tetrapods to Life in Water. Verlag Dr. F. Pfeil, München, pp 289–306

  • Sander M, Andrassy P (2006) Lines of arrested growth and long bone histology in Pleistocene large mammals from Germany: what do they tell us about dinosaur physiology? Palaeontograph A 277: 143–159

    Google Scholar 

  • Savage RJG (1977) Review of early Sirenia. Syst Zool 25: 344–351

    Article  Google Scholar 

  • Sickenberg O (1931) Morphologie und Stammesgeschichte der Sirenen. Palaeobiologica 4: 405–444

    Google Scholar 

  • Stein BR (1989) Bone density and adaptation in semi-aquatic mammals. J Mammal 70(3): 467–476

    Article  Google Scholar 

  • Väänanen HK, Laitala-Leinonen T (2008) Osteoclast lineage and function. Arch Biochem Biophys 473: 132–138

    Article  PubMed  Google Scholar 

  • Vernejoul MC de, Bénichou O (2001) Human osteopetrosis and other sclerosing disorders: recent genetic developments. Calcif Tissue Int 69: 1–6

    Google Scholar 

  • Wall WP (1983) The correlation between high limb-bone density and aquatic habits in Recent mammals. J Paleontol 57(2): 197–207.

    Google Scholar 

  • Wiffen J, Buffrénil V de, Ricqlès A de, Mazin J-M (1995) Ontogenetic evolution of bone structure in Late Cretaceous Plesiosauria from New Zealand. Geobios 28 (5): 625–640

    Google Scholar 

  • Zalmout IS, Ul-Haq M, Gingerich P (2003) New species of Protosiren (Mammalia, Sirenia) from the early middle Eocene of Balochistan (Pakistan). Contrib Mus Pal Univ Michigan 31(3): 79–87

    Google Scholar 

  • Zangerl R (1935) Pachypleurosaurus edwardsi Cornalia. Osteologie, Variationsbreite, Biologie. Die Triasfauna der Tessiner Kalkalpen. Mém Soc Pal Suisse 56: 1–8

    Google Scholar 

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Acknowledgments

All persons and institutions who have lent or given specimens for this study are thanked. This includes R. Ziegler from the Staatliches Museum für Naturkunde in Stuttgart, D. Berthet from the Centre de Conservation et d’Etude des Collections du Muséum de Lyon, and C. Lefèvre who facilitated access to the osteological collections of comparative anatomy of the Muséum National d’Histoire Naturelle, Paris. Furthermore, the authors are very grateful to H. Lamrous and M. Lemoine for some histological preparations and are indebted to A. Houssaye for her technical aid.

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Authors and Affiliations

  1. Département Histoire de la Terre, UMR 7207 (CR2P), Muséum National d’Histoire Naturelle, Bâtiment de Géologie CC 48, 57 rue Cuvier, Paris, F-75005, France

    Vivian de Buffrénil & Aurore Canoville

  2. Faculty of Medicine (Section of Anthropology), State University of Chieti, Trento e Trieste, Chieti, Italy

    Ruggero D’Anastasio

  3. Department of Anatomy (Laboratory of Evolutionary Biology), Howard University, Washington, DC, USA

    Daryl P. Domning

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  1. Vivian de Buffrénil
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  2. Aurore Canoville
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  3. Ruggero D’Anastasio
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  4. Daryl P. Domning
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Correspondence to Vivian de Buffrénil.

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de Buffrénil, V., Canoville, A., D’Anastasio, R. et al. Evolution of Sirenian Pachyosteosclerosis, a Model-case for the Study of Bone Structure in Aquatic Tetrapods. J Mammal Evol 17, 101–120 (2010). https://doi.org/10.1007/s10914-010-9130-1

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  • DOI: https://doi.org/10.1007/s10914-010-9130-1

Keywords

  • Sirenia
  • Bone
  • Histology
  • Osteosclerosis
  • Pachyostosis
  • Evolution