A microanatomical and histological study of the postcranial dermal skeleton in the Devonian sarcopterygian Eusthenopteron foordi

• Autorzy: Zylberberg L , Meunier F.J. , Laurin M.
• Języki publikacji: EN

Abstrakty

EN

The fin rays and two types of scales (enlarged and regular) of the Devonian sarcopterygian Eusthenopteron foordi are redescribed using light, scanning and transmission electron microscopy. The fin rays consist of lepidotrichia composed of ossified, jointed and branched segment pairs. The basal segments are cylindrical, but more distal elements are crescentic in section. The distribution of Sharpey’s fibres varies along the lepidotrichia. In the proximal segments, lateral bundles form a belt connecting adjacent hemisegments. In the distal segments, thin bundles are restricted to the area facing the fin surface. Both enlarged and regular scales have a similar spatial organisation. They are composed of a superficial highly mineralised layer covering a thick basal plate where the fibrils are distributed in superimposed strata forming a plywood−like structure. Nevertheless, the enlarged and regular scales differ in their shape, in the mineralised tissues of the superficial layer, and in the organisation of the plywood−like structure. The superficial layer of the enlarged scales is composed of parallel−fibered bone covering a deeper layer of woven−fibered bone. The basal plate is made of an orthogonal plywood−like structure. The thin, lamellar, imbricated regular scales display the characteristics of elasmoid scales. The mineralised tissue forming the superficial layer resembles that of extant teleost scales. In the basal plate, the twisted plywood−like structure is composed of closely packed fibrils that are preserved down to the ultrastructural level owing to the persistence of bridges connecting the fibrils. The enlarged and the regular scales of Eusthenopteron foordi do not present superficial odontodes, in contrast to ancestral thick rhomboid scales. The disappearance of enamel/enameloid and dentine may be related to the evolutionary trend towards a lightening of the dermal skeleton that would improve the swimming abilities of the animal. The characteristics of the dermal skeleton of Eusthenopteron foordi support the hypothesis that this process began early in osteichthyans.

Słowa kluczowe

EN

paleontology; microanatomical study; histology; postcranial dermal skeleton; Devonian; sarcopterygian; Eusthenopteron foordi; Sarcopterygii; Tetrapodomorpha; Tristichopteridae; Eusthenopteron; elasmoid scale; paleohistology; transmission electron microscopy; Late Devonian; Frasnian; fossil record

• Wydawca: -
• Czasopismo: Acta Palaeontologica Polonica
• Rocznik: 2010
• Tom: 55
• Numer: 3
• Opis fizyczny: p.459-470,fig.,ref.

Twórcy

autor

Zylberberg L

• Universite Pierre et Marie Curie, ISTEP, Equipe Biomineralisations et Paleoenvironnements, 4 place Jussieu, BC19, 75252 Paris c.05, France

autor

Meunier F.J.

autor

Laurin M.

Bibliografia

• Andrews, S.M. 1985. Rhizodont crossopterygian fish from the Dinantian of Foulden, Berwickshire, Scotland, with a re−evaluation of this group. Transactions of the Royal Society of Edinburgh 76: 67–95.
• Andrews, S.M. and Westoll, T.S. 1970. The postcranial skeleton of Eusthenopteron foordi Whiteaves. Transactions of the Royal Society of Edinburgh 68: 207–329.
• Beccera, J., Montes, G.S., Bexiga, S.R.R., and Junqueira, L.C.U. 1983. Structure of the tail fin in teleosts.Cell Tissue Research 230:127–137.
• Bertin, L. 1944. Modifications proposées dans la nomenclature des écailles et des nageoires.Bulletin de la Société Zoologique de France 69: 198–202.
• Burdak, V.D. 1986. Morphologie fonctionnelle du tégument écailleux des poissons. Cybium (Supplement 10). 147 pp. (French translation, from Russian, in: La pensée scientifique, Kiev, 1979).
• Castanet, J., Meunier, F., Bergot, C., and François, Y. 1975. Données préliminaires sur les structures histologiques du squelette de Latimeria chalumnae. I. Dents, écailles, rayons de nageoires. In: CNRS (ed.), Problèmes actuels de Paléontologie – Evolution des Vertébrés. Colloque International C.N.R.S, N218 (Paris, 4–9 juin 1973), 159–168. C.N.R.S., Paris.
• Clack, J.A. 2002. Gaining Ground: the Origin and Evolution of Tetrapods. 369 pp. Indiana University Press, Bloomington.
• Cloutier, R. 1996. Taxonomic review of Eusthenopteron foordi. In: H.P. Schultze and R. Cloutier (eds.), Devonian fishes and plants of Miguasha, Quebec, Canada, 271–315. Verlag Dr. Friedrich Pfeil, München.
• Cote, S., Carroll, R., Cloutier, R., and Bar−Sach, L. 2002. Vertebral development in the Devonian sarcopterygian fish Eusthenopteron foordi and the polarity of vertebral evolution in non−amniote tetrapods. Journal Vertebrate Paleontology 22: 487–502. http://dx.doi.org/10.1671/0272-4634 (2002)022%5B0487:VDITDS%5D2.0.CO;2
• Daget, J. Gayet, M., Meunier, F.J., and Sire, J.Y. 2001. Major discoveries on the dermal skeleton of fossil and recent polypteriforms: a review. Fish and Fisheries 2: 113–124. http://dx.doi.org/10.1046/j.1467-2960.2001.00046.x
• Davis, M.C., Shubin, N.H., and Daeschler, E.B. 2001. Immature rhizodontids from the Devonian of North America. Bulletin of the Museum of Comparative Zoology 156: 171–187.
• Davis, M.C., Shubin, N.H., and Daeschler, E.B. 2004. A new specimen of Sauripterus taylor (Sarcopterygii, Osteichthyes) from the Famennian Catskill Formation of North America. Journal of Vertebrate Paleontology 24: 26–40. http://dx.doi.org/10.1671/1920-3
• Dias, E.V. and Richter, M. 2002. On the squamation of Australerpeton cosgriffi Barberena, a temnospondyl amphibian from the Upper Permian of Brazil. Anais da Academia Brasileira de Ciencias 74: 477–490. http://dx.doi.org/10.1590/S0001-37652002000300010
• Doberenz, A.R. and Wickoff, W.G. 1967. Fine structure in fossil collagen. Proceedings of National Academy of Science USA 57: 539–541. http://dx.doi.org/10.1073/pnas.57.3.539
• Fawcett, D.W. 1994. Bloom and Fawcett. A Textbook of Histology. 12th edition. 988 pp. Chapman and Hall, Philadelphia.
• Francillon−Vieillot, H., Buffrénil, V. de, Castanet, J., Géraudie, J., Meunier, F.J., Sire, J.Y, Zylberberg, L., and Ricqlès, A. de 1990. Microstructure and mineralization of Vertebrate skeletal tissues. In: J.G. Carter (ed.), Skeletal biomineralization: patterns, processes and evolutionary trends. Vol. 1, 471–530. Van Nostrand Reinhold, New York.
• Géraudie, J. 1988. Fine structural peculiarities of the pectoral fin dermoskeleton of two Brachiopterygii Polypterus senegalus and Calamoichthys calabaricus (Pisces, Osteichthyes). Anatomical Record 221:455–468. http://dx.doi.org/10.1002/ar.1092210102
• Géraudie, J. and Meunier, F.J. 1982. Comparative fine structure of the osteichthyan dermotrichia. Anatomical Record 202: 325–328. http://dx.doi.org/10.1002/ar.1092020304
• Géraudie, J. and Meunier, F.J. 1984. Structure and comparative morphology of camptotrichia of lungfish fins. Tissue and Cell 16: 217–236. http://dx.doi.org/10.1016/0040-8166(84)90046-6
• Giraud, M.M., Castanet, J., Meunier, F.J., and Bouligand,Y. 1978. The fibrous structure of coelacanth scales: a twisted “plywood”. Tissue and Cell 10: 671–686. http://dx.doi.org/10.1016/0040-8166(78)90054-X
• Goodrich, E.S. 1904. On the dermal fin−rays of fishes: living−extinct. Quarterly Journal of Microscopical Research 47: 465–521.
• Goodrich, E.S. 1907. On the scales of fish living and extinct, and their importance in classification. Proceedings of the Zoological Society London 2: 751–774.
• Hadiaty, R.K. and Rachmatika, I. 2003. Morphological study of Latimeria menadoensis scales. Treubia 33: 1–11.
• Janvier, P. 1996. Early Vetebrates. Oxford Monographs on Geology and Geophysics 33: 1–393.
• Jarvik, E. 1944. On the exoskeletal shoulder girdle of the teleostomian fishes with special reference to Eusthenopteron foordi Whiteaves. Kungliga Svenska Vetenskapsakademiens Handlingar 21: 1–32.
• Jarvik, E. 1959. Dermal fins and Holmgren’s principle of delamination. Kungliga Svenska Vetenskapsakademiens Handlingar 6: 3–51.
• Jarvik, E. 1965. On the origin of girdles and paired fins.Israel Journal of Zoology 14: 141–172.
• Jeffery, J.E. 2001. Pectoral fins of rhizondontids and the evolution of pectoral appendages in tetrapod stem−group. Biological Journal of the Linnean Society 74: 217–236. http://dx.doi.org/10.1111/j.1095-8312.2001.tb01388.x
• Johanson, Z., Burrow, C., Warren, A., and Garvey, J. 2005. Homology of fin lepidotrichia in osteichthyan fishes. Lethaia 38: 27–36. http://dx.doi.org/10.1080/00241160510013141
• Kemp, A. 2002. Amino acid residues in conodont elements. Journal of Paleontology 76: 518–528. http://dx.doi.org/10.1666/0022-3360(2002)076%3C0518:AARICE%3E2.0.CO;2
• Khemiri, S., Meunier, F.J., Laurin, M., and Zylberberg, L. 2001. Morphology and structure of the scales in the Gadiformes (Actinopterygii: Teleostei: Paracantopterygii) and a comparison to the elasmoid scales of other Teleostei. Cahiers de Biologie Marine 42: 345–362.
• Landis, W. and Géraudie, J. 1990. Organization and development of the mineral during early ontogenesis of the bony fin rays of the trout Oncorhynchus mykiss. Anatomical Record 228: 383–391. http://dx.doi.org/10.1002/ar.1092280404
• Lanzing, W.J.R. 1976. The fine structure of fins and finrays of Tilapia mossambica (Peters). Cell and Tissue Research 173: 349–356. http://dx.doi.org/10.1007/BF00220323
• Laurin, M. 1998. A reevaluation of the origin of pentadactyly. Evolution 52: 1476–1482. http://dx.doi.org/10.2307/2411316
• Laurin, M., Meunier, F.J., Germain, D., and Lemoine, M. 2007. A microanatomical study of the paired fin skeleton of the Devonian sarcopterygian Eusthenopteron foordi. Journal of Paleontology 8: 143–153. http://dx.doi.org/10.1666/0022-3360(2007)81%5B143:AMAHSO%5D2.0.CO;2
• Marjanović, D. and Laurin, M. 2009. The origin(s) of modern amphibians: a commentary. Evolutionary Biology 36: 336–338. http://dx.doi.org/10.1007/s11692-009-9065-8
• Meinke, D.H. 1984. A review of cosmine: its structure, development, and relationship to other forms of the dermal skeleton of osteichthyans. Journal of Vertebrate Paleontology 4: 457–470.
• Meunier, F.J. 1980. “Twisted plywood” structure and mineralization in the scales of a primitive living fish Amia calva. Tissue and Cell 13: 165–171. http://dx.doi.org/10.1016/0040-8166(81)90046-X
• Meunier, F.J. 1984. Spatial organization and mineralisation of the basal plate of elasmoid scales in osteichthyans. American Zoologist 24: 953–964.
• Meunier, F.J. 1987. Os cellulaire, os acellulaire et tissus dérivés chez les ostéichthyens: les phénomènes de l’acellularisation et de la perte de la minéralisation. Annales de Biologie 26: 201–233.
• Meunier, F.J. and Brito, P.M. 2004. Paleohistology of basal teleostean scales. Cybium 28: 225–235.
• Meunier, F.J. and François, Y. 1980. L’organisation spatiale des fibres collagènes et la minéralisation des écailles des Dipneustes actuels. Bulletin de la Société Zoologique de France 195: 215–226.
• Meunier, F. and Poplin, C. 1995. Paleohistological study of the scales of Amia robusta Priem 1901, Amiidae from the Thanetian (Paleocene) of Cernay (France). Geobios 28 (Supplement 2): 39–43. http://dx.doi.org/10.1016/S0016-6995(95)80084-0
• Meunier, F.J. and Zylberberg, L. 1999. The structure of the external layer and of the odontodes of scales in Latimeria chalumnae (Sarcopterygii, Actinistia, Coelacanthidae) revisited using scanning and transmission electron microscopy. In: B. Séret and J.−Y. Sire (eds.), Proceedings of the 5th Indo−Pacific Fish Conference Nouméa, 1997, 109–116. Société Française d’Ichtyologie, Paris.
• Meunier, F.J., Erdmann, M.V., Fermon, Y., and Caldwell, R.L. 2008. Can the comparative study of the morphology and histology of the scales of Latimeria menadoensis and L. chalumnae (Sarcopterygii: Actinistia, Coelacanthidae) bring new insight on the taxonomy and the biogeography of recent coelacanthids? In: L. Cavin, A. Longbottom, and M. Richter (eds.), Fishes and the break−up of the Pangoea. Geological Society of London, Special Publications 29: 351–360.
• Miller, W.A. 1979. Observations on the structure of mineralized tissue of the coelacanth, including scales and their associate odontodes.In: The Biology and Physiology of the living Coelacanth. Occasional Papers of the California Academy of Sciences 134: 68–78.
• Ørvig, T. 1951. Histologic studies of placoderms and fossil elasmobranchs. 1: The endoskeleton, with remarks on the hard tissues of lower vertebrates in general. Arkiv för Zoologie 2: 321–456.
• Ørvig, T. 1957. Remarks on the vertebrate fauna of the lower Upper Devonian of Escuminac Bay, P.Q., Canada, with special reference to the porolepiform crossopterygians. Arkiv för Zoologie 10: 367–426.
• Ørvig, T. 1968. The dermal skeleton: general consideration. In: T. Ørvig (ed.), Current Problem of Lower Vertebrate Phylogeny, Proceedings 4th Nobel Symposium, 373–397. Almqvist and Wiksell, Stockholm. Ørvig, T. 1969. Cosmine and cosmine growth. Lethaia 2: 141–260.
• Otto, M. and Laurin, M. 1999. Osteostracan tesserae from the Baltic Middle Devonian: morphology and microanatomy. Neues Jahrbuch für Geologie und Paläontologie, Monatsshefte 1999: 464–476.
• Otto, M. and Laurin, M. 2001a. Taxonomic note on osteostracan tesserae from the Baltic Middle Devonian. Neues Jahrbuch für Geologie und Paläontologie, Monatsshefte 2001: 142–144.
• Otto, M. and Laurin, M. 2001b. Microanatomy of the dermal skeleton of Balticaspis latvica (Osteostraci, Middle Devonian). Journal of Vertebrate Paleontology 21: 186–189. http://dx.doi.org/10.1671/0272-4634(2001)021%5B0186:MOTDSO%5D2.0.CO;2
• Pawlicki, R., Korbel, A., and Kubiac, H. 1966. Cell, collagen fibrils and vessels in dinosaur bone. Nature 211: 1502–1503. http://dx.doi.org/10.1038/211655a0
• Rimblot−Baly, F., Ricqlès A. de, and Zylberberg, L. 1995. Analyse paléohistologique d’une série de croissance partielle chez Lappentosaurus madagascariensis (Jurassique moyen): Essai sur la dynamique de croissance d’un dinosaure sauropode. Annales de Paléontologie 81: 49–86.
• Ruta, M. and Coates, M.I. 2007. Dates, nodes and character conflict: addressing the lissamphibian origin problem. Journal of Systematic Paleontology 5: 69–122. http://dx.doi.org/10.1017/S1477201906002008
• Schaeffer, B. 1977. The dermal skeleton in fishes. In: S.M. Andrews, R.S. Miles, and A.D. Walker (eds.), Problems in Vertebrate Evolution, 25–52. Academic Press, London.
• Scheyer, T.M. and Sander, P.M. 2009. Bone microstructures and mode of skeletogenesis in osteoderms of three pareiasaur taxa from the Permian of South Africa. Journal of Evolutionary Biology 22: 1153–1162. http://dx.doi.org/10.1111/j.1420-9101.2009.01732.x
• Schönbörner, A.A., Boivin, G., and Baud, C.A. 1979. The mineralization processes in teleost fish scales. Cell Tissue Research 202: 203–212.
• Schönbörner, A.A., Meunier, F.J., and Castanet, J. 1981. The fine structure of calcified Mandl’s corpuscules in teleost fish scales. Tissue and Cell 13: 589–597. http://dx.doi.org/10.1016/0040-8166(81)90029-X
• Schultze, H.P. 1977. Ausgansform und Entwicklung der rhombischen Schuppen der Osteichthyes (Pisces). Paläontologische Zeitschrift 51: 152–168.
• Schultze, H.−P. 1984. Juvenile specimens of Eusthenopteron foordi Whiteaves, 1881 (Osteolepiform rhipidistian, Pisces) from the Late Devonian of Miguasha, Quebec. Canadian Journal of Vertebrate Paleontology 4: 1–16.
• Schweitzer, M.H., Avci, R., Collier, T., and Goodwin, M.B. 2008. Microscopic, chemical and molecular methods for examining fossil preservation. Compte Rendus Palevol 7: 159–184. http://dx.doi.org/10.1016/j.crpv.2008.02.005
• Service, R. F. 2009. “Protein” in 80−million−year−old fossil bolsters controversial T. rex claim. Science 324: 578. http://dx.doi.org/10.1126/science.324_578
• Sire, J.Y., Donoghue P.C.J., and Vickaryous, M.K. 2009. Origin and evolution of the integumentary skeleton in non−tetrapod vertebrates. Journal of Anatomy 214: 409–440. http://dx.doi.org/10.1111/j.1469-7580.2009.01046.x
• Smith, M.M., Hobdell, M.H., and Miller, W.A. 1972. The structure of the scales of Latimeria chalumnae. Journal of Zoology, London 167: 501–509. http://dx.doi.org/10.1111/j.1469-7998.1972.tb01741.x
• Thomson, KS. 1975. On the biology of cosmine. Bulletin of the Yale Peabody Museum of Natural History 40: 1–62.
• Vickaryous, M.K. and Sire, J.Y. 2009. The integumentary skeleton of tetrapods: origin, evolution, and evolution. Journal of Anatomy 214: 441–464. http://dx.doi.org/10.1111/j.1469-7580.2008.01043.x
• Vogel, K.G. 1994. Glycosaminoglycans and proteoglycans. In: P.D. Yurchenco, D. Birk, and R.P. Mecham (eds.), Extracellular Matrix Assembly and Structure, 243–279. Academic Press, San Diego, New York.
• Witzmann, F. 2007. The evolution of the scalation pattern in temnospondyl amphibians. Zoological Journal of the Linnean Society 150: 815–834. http://dx.doi.org/10.1111/j.1096-3642.2007.00309.x
• Zocco, T.G. and Schwartz, H.L. 1994. Microstructural analysis of bone of the sauropod dinosaur Seismosaurus by transmission electron microscopy. Paleontology 37: 493–503.
• Zylberberg, L. 1988. Ultrastructural data on the scales of the dipnoan Protopterus annectens (Sarcopterygii, Osteichthyes). Journal of Zoology, London 216: 55–71. http://dx.doi.org/10.1111/j.1469-7998.1988.tb02415.x
• Zylberberg, L. and Nicolas, G. 1982. Ultrastructure of scales in a teleost (Carassius auratus L.) after use of rapid freeze−fixation and freeze−substitution. Cell Tissue Research 223: 349–367. http://dx.doi.org/10.1007/BF01258495
• Zylberberg, L. and Wake, M.H. 1990. Structure of the scales of Dermophis and Microcaecilia (Amphibia: Gymnophiona), and comparison to dermal ossification of other vertebrates. Journal of Morphology 206: 25–43. http://dx.doi.org/10.1002/jmor.1052060104
• Zylberberg, L., Castanet, J., and Ricqlès A. de 1980. Structure of the dermal scales in Gymnophiona (Amphibia). Journal of Morphology 165: 41–54. http://dx.doi.org/10.1002/jmor.1051650105
• Zylberberg, L., Géraudie, J., Meunier, F.J., and Sire, J.Y. 1992. Biomineralization in the integumental skeleton of the living lower Vertebrates. In: B.K. Hall (ed.), Bone, Vol. 4, 171–224. CRC Press, Boca Raton.