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Long-bone development and life-history traits of the Devonian tristichopterid Hyneria lindae

Published online by Cambridge University Press:  03 December 2018

Viktoriia KAMSKA ,
Edward B. DAESCHLER ,
Jason P. DOWNS ,
Per E. AHLBERG ,
Paul TAFFOREAU  and
Sophie SANCHEZ
Viktoriia KAMSKA
Affiliation:
Department of Organismal Biology, Evolution and Development, Science for Life Laboratory and Uppsala University, Norbyvägen 18A, 75236 Uppsala, Sweden. Email: sophie.sanchez@ebc.uu.se
Edward B. DAESCHLER
Affiliation:
Academy of Natural Sciences of Drexel University, 1900 Benjamin Franklin Parkway, Philadelphia, PA 19103, USA.
Jason P. DOWNS
Affiliation:
Academy of Natural Sciences of Drexel University, 1900 Benjamin Franklin Parkway, Philadelphia, PA 19103, USA. Department of Biology, Delaware Valley University, 700 East Butler Avenue, Doylestown, PA 18901, USA.
Per E. AHLBERG
Affiliation:
Department of Organismal Biology, Evolution and Development, Science for Life Laboratory and Uppsala University, Norbyvägen 18A, 75236 Uppsala, Sweden. Email: sophie.sanchez@ebc.uu.se
Paul TAFFOREAU
Affiliation:
European Synchrotron Radiation Facility, 71 avenue des Martyrs, 38000 Grenoble, France.
Sophie SANCHEZ*
Affiliation:
Department of Organismal Biology, Evolution and Development, Science for Life Laboratory and Uppsala University, Norbyvägen 18A, 75236 Uppsala, Sweden. Email: sophie.sanchez@ebc.uu.se European Synchrotron Radiation Facility, 71 avenue des Martyrs, 38000 Grenoble, France. Sorbonne Université, Centre de Recherche sur la Paléobiodiversité et les Paléoenvironnements, Muséum National d'Histoire Naturelle, Centre National de la Recherche Scientifique, Université Pierre et Marie Curie, 57 rue Cuvier, CP38, 75005 Paris, France.
*
*Corresponding author
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Abstract

Hyneria lindae is one of the largest Devonian sarcopterygians. It was found in the Catskill Formation (late Famennian) of Pennsylvania, USA. The current study focuses on the palaeohistology of the humerus of this tristichopterid and supports a low ossification rate and a late ossification onset in the appendicular skeleton. In addition to anatomical features, the large size of the cell lacunae in the cortical bone of the humerus mid-shaft may suggest a large genome size and associated neotenic condition for this species, which could, in turn, be a partial explanation for the large size of H. lindae. The low metabolism of H. lindae revealed here by bone histology supports the hypothesis of an ambush predatory behaviour. Finally, the lines-of-arrested-growth pattern and late ossification of specimen ANSP 21483 suggest that H. lindae probably had a long juvenile stage before reaching sexual maturity. Although very few studies address the life-history traits of stem tetrapods, they all propose a slow limb development for the studied taxa despite different ecological conditions and presumably distinct behaviours. The bone histology of H. lindae would favour the hypothesis that a slow long-bone development could be a general character for stem tetrapods.

Keywords

fin evolutionstem-tetrapod developmentthree-dimensional virtual palaeohistology
Type
Articles
Information
Earth and Environmental Science Transactions of The Royal Society of Edinburgh , Volume 109 , Issue 1-2: Fossils, Function and Phylogeny: Papers on Early Vertebrate Evolution in Honour of Professor Jennifer A. Clack , March 2018 , pp. 75 - 86
Copyright
Copyright © The Royal Society of Edinburgh 2018 

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References

6. References

Ahlberg, P. E. 2019. Follow the footprints and mind the gaps: a new look at the origin of tetrapods. Earth and Environmental Science Transactions of the Royal Society of Edinburgh. DOI: 10.1017/S1755691018000695.Google Scholar
Ahlberg, P. E., Clack, J. A., Luksevics, E., Blom, H. & Zupins, I. 2008. Ventastega curonica and the origin of tetrapod morphology. Nature 453, 1199–1204.10.1038/nature06991Google Scholar
Ahlberg, P. E., Beznosov, P., Luksevics, E. & Clack, J. A. 2011. A very primitive tetrapod from the earliest Famennian of South Timan, Russia. Journal of Vertebrate Paleontology 31, 60.Google Scholar
Ahlberg, P. E. & Johanson, Z. 1997. Second tristichopterid (Sarcopterygii, Osteolepiformes) from the Upper Devonian of Canowindra, New South Wales, Australia, and phylogeny of the Tristichopteridae. Journal of Vertebrate Paleontology 17, 653–673.Google Scholar
Amprino, R. 1947. La structure du tissu osseux envisagée comme expression de différences dans la vitesse de l'accroissement. Archives de Biologie 58, 315–330.Google Scholar
Astin, T. R., Marshall, J. E. A., Blom, H. & Berry, C. M. 2010. The sedimentary environment of the Late Devonian East Greenland tetrapods. Geological Society, London, Special Publications 339, 93–109.Google Scholar
Bemis, W. E. 1984. Paedomorphosis and the evolution of the Dipnoi. Paleobiology 10, 293–307.Google Scholar
Blom, H., Clack, J. A., Ahlberg, P. E. & Friedman, M. 2007. Devonian vertebrates from East Greenland: a review of faunal composition and distribution. Geodiversitas 29, 119–141.Google Scholar
Bonett, R. M., Chippindale, P. T., Moler, P. E., Devender, R. W. V. & Wake, D. B. 2009. Evolution of gigantism in amphiumid salamanders. Plos One 4, e5615.Google Scholar
Callier, V., Clack, J. A. & Ahlberg, P. E. 2009. Contrasting developmental trajectories in the earliest known tetrapod forelimbs. Science 324, 364–367.Google Scholar
Calvi, L. M., Adams, G. B., Weibrecht, K. W., Weber, J. M., Olson, D. P., Knight, M. C., Martin, R. P., Schipani, E., Divieti, P., Bringhurst, F. R., Milner, L. A., Kronenberg, H. M. & Scadden, D. T. 2003. Osteoblastic cells regulate the haematopoietic stem cell niche. Nature 425, 841–846.Google Scholar
Castanet, J., Francillon-Vieillot, H., Meunier, F.-J. & De Ricqlès, A. 1993. Bone and individual aging. In Hall, B. K. (ed.) Bone, 245–283. Boca Raton: CRC Press.Google Scholar
Castanet, J., Francillon-Vieillot, H. & De Ricqlès, A. 2003. The skeletal histology of the Amphibia. In Heatwole, H. & Davies, M. (eds) Amphibian biology, 1598–1683. Chipping Norton: Surrey Beatty & Sons.Google Scholar
Chinsamy, A. 1997. Assessing the biology of fossil vertebrates through bone histology. Palaeontologica Africana 33, 29–35.Google Scholar
Clack, J. A. 2012. Gaining ground. Bloomington, IN: Indiana University Press.Google Scholar
Clark, J. M. 1990. The structure of vascular channel in the subchondral plate. Journal of Anatomy 171, 105–115.Google Scholar
Cloutier, R. 2010. The late Devonian Biota of the Miguasha national park UNESCO world heritage site. AAAP Search and Discovery Article 90172, 10–14.Google Scholar
Cressler, W. L., Daeschler, E. B., Slingerland, R. & Peterson, D. A. 2010. Terrestrialization in the Late Devonian: a palaeoecological overview of the Red Hill site, Pennsylvania, USA. Geological Society, London, Special Publications 339, 111–128.Google Scholar
Daeschler, E. B. 2000a. An early actinopterygian fish from the Catskill formation (Late Devonian, Famennian) in Pennsylvania, USA. Proceedings of the Academy of Natural Sciences of Philadelphia 150, 181–192.Google Scholar
Daeschler, E. B. 2000b. Early tetrapod jaws from the Late Devonian of Pennsylvanian, USA. Journal of Paleontology 74, 301–308.Google Scholar
Daeschler, E. B., Shubin, N. H., Thomson, K. S. & Amaral, W. W. 1994. A Devonian tetrapod from North America. Science 265(5172), 639–642.Google Scholar
Daeschler, E. B., Frumes, A. C. & Mullison, C. F. 2003. Groenlandaspidid placoderm fishes from the Late Devonian of North America. Records-Australian Museum 55, 45–60.10.3853/j.0067-1975.55.2003.1374Google Scholar
Daeschler, E. B., Clack, J. A. & Shubin, N. H. 2009. Late Devonian tetrapod remains from Red Hill, Pennsylvania, USA: how much diversity? Acta Zoologica 90, 306–317.Google Scholar
Daeschler, E. B. & Downs, J. P. 2018. New description and diagnosis of Hyneria lindae (Sarcopterygii, Tristichopteridae) from the Upper Devonian Catskill Formation of Pennsylvania, USA. Journal of Vertebrate Paleontology 38(3), e1448834.Google Scholar
D'Emic, M. D. & Benson, R. B. J. 2013. Measurement, variation, and scaling of osteocyte lacunae: a case study in birds. Bone 57, 300–310.Google Scholar
De Ricqlès, A., Castanet, J. & Francillon-Vieillot, H. 2004. The ‘message' of bone tissue in paleoherpetology. Italian Journal of Zoology 71, 3–12.10.1080/11250000409356599Google Scholar
Downs, J. P. & Daeschler, E. B. 2001. Variation within a large sample of Ageleodus pectinatus teeth (Chondrichthyes) from the Late Devonian of Pennsylvania, USA. Journal of Vertebrate Paleontology 21, 811–814.Google Scholar
Francillon-Vieillot, H., Buffrénil, V. D., Castanet, J., Géraudie, J., Meunier, F.-J., Sire, J.-Y., Zylberberg, L. & De Ricqlès, A. 1990. Microstructure and mineralization of vetebrate skeletal tissues. In Carter, J. G. (ed.) Skeletal biomineralization: patterns, processes and evolutionary trends, 471–530. New York: Van Nostrand Reinhold.Google Scholar
Gerber, H.-P. & Ferrara, N. 2000. Angiogenesis and bone growth. Trends in Cardiovascular Medicine 10, 223–228.Google Scholar
Gregory, T. R. 2002. Genome size and developmental complexity. Genetica 115, 131–146.Google Scholar
Haines, R. W. 1938. The primitive form of epiphysis in the long bones of tetrapods. Journal of Anatomy 72, 323–343.Google Scholar
Haines, R. W. 1942. The evolution of epiphyses and of endochondral bone. Biological Review 174, 267–292.Google Scholar
Jarvik, E. 1952. On the fish-like tail in the Ichthyostegid stegocephalians: with descriptions of a new stegocephalian and a new crossopterygian from the Upper Devonian of East Greenland. Meddelelser om Grønland 114, 1–90.Google Scholar
Jarvik, E. 1980. Basic structure and evolution of vertebrates. Vol. 1. London: Academic Press.Google Scholar
Johanson, Z. & Ahlberg, P. E. 1997. A new tristichopterid (Osteolepiformes: Sarcopterygii) from the Mandagery Sandstone (Late Devonian, Famennian) near Canowindra, NSW, Australia. Earth and Environmental Science Transactions of the Royal Society of Edinburgh 88, 39–68.10.1017/S0263593300002303Google Scholar
Köhler, M., Marín-Moratalla, N., Jordana, X. & Aanes, R. 2012. Seasonal bone growth and physiology in endotherms shed light on dinosaur physiology. Nature 487, 358–361.Google Scholar
Labiche, J.-C., Mathon, O., Pascarelli, S., Newton, M. A., Guilera Ferre, G., Curfs, C., Vaughan, G., Homs, A. & Fernandez Carreiras, D. 2007. The fast readout low noise camera as a versatile X-ray detector for time resolved dispersive extended X-ray absorption fine structure and diffraction studies of dynamic problems in materials science, chemistry, and catalysis. Review of Scientific Instruments 78, 091301.Google Scholar
Long, M. W. 2001. Osteogenesis and bone-marrow-derived cells. Blood Cells, Molecules and Diseases 27, 677–690.Google Scholar
Long, M. W., Robinson, J. A., Ashcraft, E. A. & Mann, K. G. 1995. Regulation of human bone marrow-derived osteoprogenitor cells by osteogenic growth factors. Journal of Clinical Investigation 95, 881–887.10.1172/JCI117738Google Scholar
Meunier, F.-J. & Laurin, M. 2012. A microanatomical and histological study of the fin long bones of the Devonian sarcopterygian Eusthenopteron foordi. Acta Zoologica 81, 143–153.Google Scholar
Organ, C. L., Shedlock, A. M., Meade, A., Pagel, M. & Edwards, S. V. 2007. Origin of avian genome size and structure in non-avian dinosaurs. Nature 446, 180–184.Google Scholar
Organ, C. L., Struble, M., Canoville, A., de Buffrénil, V. & Laurin, M. 2016. Macroevolution of genome size in sarcopterygians during the water–land transition. Comptes Rendus Palevol 15, 65–73.10.1016/j.crpv.2015.09.003Google Scholar
Ortega, F., Behonick, D. J. & Werb, Z. 2004. Matrix remodeling during endochondral ossification. Trends in Cell Biology 14, 86–93.Google Scholar
Padian, K. 2012. Evolutionary physiology: a bone for all seasons. Nature 487, 310–311.Google Scholar
Paganin, D., Mayo, S. C., Gureyev, T. E., Miller, P. R. & Wilkins, S. W. 2002. Simultaneous phase and amplitude extraction from a single defocused image of a homogeneous object. Journal of Microscopy 206, 33–40.Google Scholar
Sanchez, S., Klembara, J., Castanet, J. & Steyer, J.-S. 2008. Salamander-like development in a seymouriamorph revealed by palaeohistology. Biology Letters 4, 411–414.Google Scholar
Sanchez, S., De Ricqlès, A., Schoch, R. R. & Steyer, J.-S. 2010. Developmental plasticity of limb bone microstructural organization in Apateon: histological evidence of paedomorphic conditions in branchiosaurs. Evolution & Development 12, 315–328.Google Scholar
Sanchez, S., Ahlberg, P. E., Trinajstic, K., Mirone, A. & Tafforeau, P. 2012. Three dimensional synchrotron virtual paleohistology: a new insight into the world of fossil bone microstructures. Microscopy and Microanalysis 18, 1095–1105.10.1017/S1431927612001079Google Scholar
Sanchez, S., Dupret, V., Tafforeau, P., Trinajstic, K., Ryll, B., Gouttenoire, P.-J., Wretman, L., Zylberberg, L., Peyrin, F. & Ahlberg, P. E. 2013. 3D microstructural architecture of muscle attachments in extant and fossil vertebrates revealed by synchrotron microtomography. Plos One 8, e56992.Google Scholar
Sanchez, S., Tafforeau, P. & Ahlberg, P. E. 2014. The humerus of Eusthenopteron: a puzzling organization presaging the establishment of tetrapod limb bone marrow. Proceedings of the Royal Society of London B 281, 20140299.Google Scholar
Sanchez, S., Tafforeau, P., Clack, J. A. & Ahlberg, P. E. 2016. Life history of the stem tetrapod Acanthostega revealed by synchrotron microtomography. Nature 537, 408–411.10.1038/nature19354Google Scholar
Sanchez, S. & Schoch, R. R. 2013. Bone histology reveals a high environmental and metabolic plasticity as a successful evolutionary strategy in a long-lived homeostatic Triassic temnospondyl. Evolutionary Biology 40, 627–647.Google Scholar
Schoch, R. R. 2013. How body size and development biased the direction of evolution in early amphibians. Historical Biology 25, 155–165.Google Scholar
Schultze, H. P. & Cloutier, R. 1996. Devonian fishes and plants of Miguasha, Quebec, Canada. München: Verlag Dr. Friedrich Pfeil.Google Scholar
Sevon, W. D. 1985. Nonmarine facies of the Middle and Late Devonian Catskill coastal alluvial plain. In Woodrow, D. L. & Sevon, W. D. (eds) The Catskill Delta, 79–90. Boulder, CO: The Geological Society of America.Google Scholar
Snyder, D., Turner, S., Burrow, C. J. & Daeschler, E. B. 2017. ‘Gyracanthus' sherwoodi (gnathostomata, Gyracanthidae) from the Late Devonian of North America. Proceedings of the Academy of Natural Sciences of Philadelphia 165, 195–219.Google Scholar
Suzuki, F., Takase, T., Takigawa, M., Uchida, A. & Shimomura, Y. 1981. Simulation of the initial stage of endochondral osification: in vitro sequential culture of growth cartilage cells and bone marrow cells. Proceedings of the National Academy of Sciences 78, 2368–2372.10.1073/pnas.78.4.2368Google Scholar
Tafforeau, P., Bentaleb, I., Jaeger, J.-J. & Martin, C. 2007. Nature of laminations and mineralization in rhinoceros enamel using histology and X-ray synchrotron microtomography: potential implications for palaeoenvironmental isotopic studies. Palaeogeography, Palaeoclimatology, Palaeoecology 246, 206–227.Google Scholar
Thomson, K. S. 1968. A new Devonian fish (Crossopterygii: Rhipidistia) considered in relation to the origin of the Amphibia. Postilla 124, 1–13.Google Scholar
Thomson, K. S. 1976. The faunal relationships of rhipidistian fishes (Crossopterygii) from the Catskill (Upper Devonian) of Pennsylvania. Journal of Paleontology 50(6), 1203–1208.Google Scholar
Trueta, J. 1963. The role of the vessels in osteogenesis. Bone & Joint Journal 45, 402–418.Google Scholar
Vecoli, M., Meyer-Berthaud, B. & Clement, G. 2010. The terrestrialization process: modelling complex interactions at the biosphere-geosphere interface-Introduction. Geological Society, London, Special Publications 339, 1–3.Google Scholar
Wake, D. B. 1991. Homoplasy: the result of natural selection, or evidence of design limitations? American Naturalist 138, 543–567.Google Scholar
Webb, P. W. 1984. Body form, locomotion and foraging in aquatic vertebrates. American Zoologist 24, 107–120.Google Scholar
Wilson, A. & Trumpp, A. 2006. Bone-marrow haematopoietic-stem-cell niches. Nature Reviews – Immunology 6, 93–106.Google Scholar
Wilson, H. M., Daeschler, E. B. & Desbiens, S. 2005. New flat-backed archipolypodan millipedes from the Upper Devonian of North America. Journal of Paleontology 79, 738–744.Google Scholar
Witten, P. E. & Huysseune, A. 2007. Mechanisms of chondrogenesis and osteogenesis in fins. In Hall, B. K. (ed.) Fins into limbs: evolution, development and transformation, 79–92. Chicago, IL: University of Chicago Press.Google Scholar
Woodrow, D. L. & Sevon, W. D. 1985. The Catskill Delta. Vol. 201. Boulder, CO: Geological Society of America.Google Scholar
Young, B., Dunstone, R. L., Senden, T. J. & Young, G. C. 2013. A gigantic sarcopterygian (Tetrapodomorph Lobe-Finned Fish) from the Upper Devonian of Gondwana (Eden, New South Wales, Australia). Plos One 8, e53871.Google Scholar