Advertisement

Journal of Mammalian Evolution

, Volume 17, Issue 2, pp 101–120 | Cite as

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

  • Vivian de Buffrénil
  • Aurore Canoville
  • Ruggero D’Anastasio
  • Daryl P. Domning
Original Paper

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.

Keywords

Sirenia Bone Histology Osteosclerosis Pachyostosis Evolution 

Notes

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.

References

  1. Asagiri M, Takayanagi H (2007) The molecular understanding of osteoclast differentiation. Bone 40: 251–264CrossRefPubMedGoogle Scholar
  2. 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): 87–93Google Scholar
  3. Brandt A (1852) Dissertationes de ossificationis processu. Inaugural dissertation, Dorpat.Google Scholar
  4. Buffrénil V de, Rage J-C (1993) La “ pachyostose ” vertébrale de Simoliophis (Reptilia, Squamata) : données comparatives et considérations fonctionnelles. Ann Paléontol 79: 315–335Google Scholar
  5. 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): 455–466Google Scholar
  6. 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): 255–275Google Scholar
  7. Buffrénil V de, Schoevaert D (1988) On how the delphinid humerus becomes cancellous: ontogeny of a histological specialization. J Morphol 198: 146–164Google Scholar
  8. 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: 2107–2119Google Scholar
  9. Castanet J (2006) Time recording in bone microstructures of endothermic animals. CR Palevol 5: 629–636CrossRefGoogle Scholar
  10. Cave AJE, Aumonier FJ (1967) Observations on dugong histology. Quart J Roy Microsc Soc 87: 113–121Google Scholar
  11. Cubo J (2000) Process heterochronies in endochondral ossification. J Theor Biol 205: 343–353CrossRefPubMedGoogle Scholar
  12. D’Anastasio R (2004) Idiopathic hyperostosis: epidemiology and phylogeny. J Paleopathol 16(3): 133–145Google Scholar
  13. Domning DP (1978) Sirenian evolution in the North Pacific Ocean. Univ Calif Publ Geol Sci 118: 1–176Google Scholar
  14. ——— (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 177–189Google Scholar
  15. ——— (2000) The readaptation of Eocene sirenians to life in water. Hist Biol 14(1–2): 115–119CrossRefGoogle Scholar
  16. ——— (2001a) The earliest fully quadrupedal sirenian. Nature 413: 625–627CrossRefPubMedGoogle Scholar
  17. ——— (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 151–168Google Scholar
  18. ——— (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): 27–50Google Scholar
  19. ——— (2002) Sirenian evolution. In: Perrin WF, Wursig B, Thewissen JGM (eds) Encyclopedia of Marine Mammals. Academic Press, London, New York, pp 1083–1086Google Scholar
  20. 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): 479–500CrossRefGoogle Scholar
  21. Domning DP, Buffrénil V. de (1991) Hydrostasis in the Sirenia : quantitative data and functional interpretations. Mar Mamm Sci 7(4): 331–368Google Scholar
  22. 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): 203–207Google Scholar
  23. Fawcett DW (1942) The amedullary bones of the Florida manatee (Trichechus latirostris). Am J Anat 71: 27–309CrossRefGoogle Scholar
  24. 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 471–530Google Scholar
  25. Gallivan GJ, Best RC, Kanwisher JW (1983) Temperature regulation in the Amazonian manatee, Trichechus inunguis. Physiol Zool 56: 255–262Google Scholar
  26. 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): 41–67Google Scholar
  27. Girondot M, Laurin M (2003) Bone profiler: a tool to quantify, model, and statistically compare bone-section compactness profiles. J Vertebr Paleontol 23(2): 458–461CrossRefGoogle Scholar
  28. Gray NM, Kimberly K, Madar S, Tomko L, Wolfe S (2007) Sink or swim? Bone buoyancy control in early cetaceans. Anat Rec 290(6): 638–653CrossRefGoogle Scholar
  29. 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): 685–691Google Scholar
  30. Husar SL (1975) A review of the literature on the dugong (Dugong dugon). US Department of Interior Fish and Wildlife Service, Wildlife Research Report 4Google Scholar
  31. Irvine AB (1983) Manatee metabolism and its influence on distribution in Florida. Biol Conserv 25: 315–334CrossRefGoogle Scholar
  32. Kaiser HE (1960) Untersuchungen zur vergleichenden Osteologie der fossilen und rezenten Pachyostosen. Palaeontograph A 114(5–6): 113–196Google Scholar
  33. ——— (1970) Das Abnorm in der Evolution. Acta Biotheor, suppl 9. E.J. Brill, Leyden.Google Scholar
  34. Karsenty G (2007) The genetic transformation of bone biology. Genes Develop 13: 3037–3051CrossRefGoogle Scholar
  35. 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 1217–1227Google Scholar
  36. Kiprijanoff AV (1881–1883) Studien über die fossilen Reptilien Russlands. Mém Acad Imp Sci Saint Petersbourg 7: 1–144Google Scholar
  37. Klevezal GA (1996) Recording Structures of Mammals: Determination of Age and Reconstruction of Life History. Balkema, Rotterdam.Google Scholar
  38. Laurin M, Girondot M, Loth M-M (2004) The evolution of long bone microstructure and lifestyle in lissamphibians. Paleobiology 30(4): 589–613CrossRefGoogle Scholar
  39. Madar SI (2007) The postcranial skeleton of early Eocene pakicetid cetaceans. J Paleontol 81(1): 176–200CrossRefGoogle Scholar
  40. 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): 54–88CrossRefGoogle Scholar
  41. 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): 181–201Google Scholar
  42. Marsh H, Spain AV, Heinsohn GE (1978) Minireview. Physiology of the dugong. Comp Biochem Physiol A61: 159–168CrossRefGoogle Scholar
  43. Meister W (1962) Histological structure of the long bones of penguins. Anat Rec 143: 377–386CrossRefPubMedGoogle Scholar
  44. Nopcsa F von (1923) Vorläufige Notiz über die Pachyostose und Osteosklerose einiger mariner Wirbeltiere. Anat Anz 56: 353–359Google Scholar
  45. Nopcsa F von, Heidsieck E (1934) Über eine pachyostotische Rippe aus der Kreide Rügens. Acta Zool (Stockholm) 15: 431–455Google Scholar
  46. 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: 1–6CrossRefGoogle Scholar
  47. Pilleri G, Biosca J, Via L 1989. The Tertiary Sirenia of Catalonia. Brain Anatomy Institute, University of Berne, Ostermundigen (Berne)Google Scholar
  48. Popoff SN, Marks SC (1995) The heterogeneity of the osteopetroses reflects the diversity of cellular influences during skeletal development. Bone 17(5): 437–445CrossRefPubMedGoogle Scholar
  49. 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: 51–129Google Scholar
  50. ——— (1989) Les mécanismes hétérochroniques dans le retour des tétrapodes au milieu aquatique. Geobios, mém spéc 12: 337–348Google Scholar
  51. 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: 47–53Google Scholar
  52. ——— (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 289–306Google Scholar
  53. 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: 143–159Google Scholar
  54. Savage RJG (1977) Review of early Sirenia. Syst Zool 25: 344–351CrossRefGoogle Scholar
  55. Sickenberg O (1931) Morphologie und Stammesgeschichte der Sirenen. Palaeobiologica 4: 405–444Google Scholar
  56. Stein BR (1989) Bone density and adaptation in semi-aquatic mammals. J Mammal 70(3): 467–476CrossRefGoogle Scholar
  57. Väänanen HK, Laitala-Leinonen T (2008) Osteoclast lineage and function. Arch Biochem Biophys 473: 132–138CrossRefPubMedGoogle Scholar
  58. Vernejoul MC de, Bénichou O (2001) Human osteopetrosis and other sclerosing disorders: recent genetic developments. Calcif Tissue Int 69: 1–6Google Scholar
  59. Wall WP (1983) The correlation between high limb-bone density and aquatic habits in Recent mammals. J Paleontol 57(2): 197–207.Google Scholar
  60. 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): 625–640Google Scholar
  61. 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): 79–87Google Scholar
  62. Zangerl R (1935) Pachypleurosaurus edwardsi Cornalia. Osteologie, Variationsbreite, Biologie. Die Triasfauna der Tessiner Kalkalpen. Mém Soc Pal Suisse 56: 1–8Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • Vivian de Buffrénil
    • 1
  • Aurore Canoville
    • 1
  • Ruggero D’Anastasio
    • 2
  • Daryl P. Domning
    • 3
  1. 1.Département Histoire de la Terre, UMR 7207 (CR2P)Muséum National d’Histoire NaturelleParisFrance
  2. 2.Faculty of Medicine (Section of Anthropology)State University of ChietiChietiItaly
  3. 3.Department of Anatomy (Laboratory of Evolutionary Biology)Howard UniversityWashingtonUSA

Personalised recommendations