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Original article : anatomy atlas
MicroCT survey of larval skeletal mineralization in the Cuban gar Atractosteus tristoechus (Actinopterygii; Lepisosteiformes)
Published online: 17/05/2017
Keywords:
Actinopterygii; development; Lepisosteiformes; mineralization; skeleton
https://doi.org/10.18563/m3.3.3.e3
References: 63 Cited by: 4
Cite this article:
Raphaël Scherrer, Andrés Hurtado, Erik Garcia Machado and Mélanie Debiais-Thibaud, 2017. MicroCT survey of larval skeletal mineralization in the Cuban gar Atractosteus tristoechus (Actinopterygii; Lepisosteiformes). MorphoMuseuM 3 (3)-e3. doi: 10.18563/m3.3.3.e3
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Abstract
Using X-ray microtomography, we describe the ossification events during the larval development of a non-teleost actinopterygian species: the Cuban gar Atractosteus tristoechus from the order Lepisosteiformes. We provide a detailed developmental series for each anatomical structure, covering a large sequence of mineralization events going from an early stage (13 days post-hatching, 21mm total length) to an almost fully ossified larval stage (118dph or 87mm in standard length). With this work, we expect to bring new developmental data to be used in further comparative studies with other lineages of bony vertebrates. We also hope that the on-line publication of these twelve successive 3D reconstructions, fully labelled and flagged, will be an educational tool for all students in comparative anatomy.
Specimens and 3D Data
Atractosteus tristoechus At1-13dph
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Atractosteus tristoechus At2-16dph
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Atractosteus tristoechus At3-19dph
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Atractosteus tristoechus At4-22dph
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Atractosteus tristoechus At5-26dph
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Atractosteus tristoechus At6-31dph
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Atractosteus tristoechus At7-37dph
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Atractosteus tristoechus At8-52dph
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Atractosteus tristoechus At9-74dph
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Atractosteus tristoechus At10-89dph
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M3#103 Atractosteus tristoechus larva, 89 dph, 63mm SL.
Not all structures are colored, only newly ossified ones.
You may find the tag file in the At1-13dph reconstruction data. Type: "3D_surfaces"
doi: 10.18563/m3.sf.103
state:published |
Download 3D surface file
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Atractosteus tristoechus At11-104dph
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Atractosteus tristoechus At12-118dph
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Published in Volume 03, Issue 03 (2017)
References
Arratia, G., 2009. Identifying patterns of diversity of the actinopterygian fulcra. Acta Zoologica. 90, 220–235. https://doi.org/10.1111/j.1463-6395.2008.00375.x
Arratia, G., Schultze, H.-P., 1991. Palatoquadrate and Its Ossifications: Development and Homology Within Osteichthyans. Journal of Morphology. 208, 1–81. https://doi.org/10.1002/jmor.1052080102
Arratia, G., Schultze, H.-P., 1992. Reevaluation of the caudal skeleton of certain actinopterygian fishes: III. Salmonidae. Homologization of caudal skeletal structures. Journal of Morphology. 214, 187–249. https://doi.org/10.1002/jmor.1052140209
Betancur-R, R., Broughton, R.E., Wiley, E.O., Carpenter, K., López, J.A., Li, C., Holcroft, N.I., Arcila, D., Sanciangco, M., Ii, J.C.C., Zhang, F., Campbell, M.A., Ballesteros, J.A., Roa-varon, A., Willis, S., Borden, W.C., Hough, D.J., Lu, G., 2013. The Tree of Life and a New Classification of Bony Fishes. PLOS Currents Tree of Life. 732988, 1–45. https://doi.org/10.1371/currents.tol.53ba26640df0ccaee75bb165c8c26288
Boughner, J.C., Buchtová, M., Fu, K., Diewert, V., Hallgrímsson, B., Richman, J.M., 2007. Embryonic development of Python sebae - I: Staging criteria and macroscopic skeletal morphogenesis of the head and limbs. Zoology. 110, 212–230. https://doi.org/10.1016/j.zool.2007.01.005
Britz, R., Johnson, G.D., 2010. Occipito-vertebral fusion in actinopterygians: conjecture, myth and reality. Part 1: Non-teleosts. In: Mesozoic Fishes 4-Homology and Phylogeny. J. S. Nelson, H.-P. Schultze, and M. V. H. Wilson (Eds.). Verlag Dr. Freidrich Pfeil, München. pp. 77–93.
Broughton, R.E., Betancur-R., R., Li, C., Arratia, G., Ortí, G., 2013. Multi-locus phylogenetic analysis reveals the pattern and tempo of bony fish evolution, PLoS Currents Tree of Life. https://doi.org/10.1371/currents.tol.2ca8041495ffafd0c92756e75247483e
Cignoni, P., Cignoni, P., Callieri, M., Callieri, M., Corsini, M., Corsini, M., Dellepiane, M., Dellepiane, M., Ganovelli, F., Ganovelli, F., Ranzuglia, G., Ranzuglia, G., 2008. MeshLab: an Open-Source Mesh Processing Tool. Sixth Eurographics Italian Chapter Conference. 129–136.
Dean, M.N., Mull, C.G., Gorb, S.N., Summers, A.P., 2009. Ontogeny of the tessellated skeleton: Insight from the skeletal growth of the round stingray Urobatis halleri. Journal of Anatomy. 215, 227–239. https://doi.org/10.1111/j.1469-7580.2009.01116.x
Dufeau, D.L., Witmer, L.M., 2015. Ontogeny of the Middle-Ear Air-Sinus System in Alligator mississippiensis (Archosauria: Crocodylia). PLoS ONE. 10, 1–25. https://doi.org/10.1371/journal.pone.0137060
Enault S., Adnet S., Debiais-Thibaud M., 2016. Skeletogenesis during the late embryonic development of the catshark Scyliorhinus canicula (Chondrichthyes; Neoselachii). MorphoMuseuM 1 (4)-e2. https://doi.org/10.18563/m3.1.4.e2
Friedman, M., 2015. The early evolution of ray-finned fishes. Palaeontology. 58, 213–228. https://doi.org/10.1111/pala.12150
Gardiner, B.G., Littlewood, D.T.G., Maisey, J.G., 1996. Interrelationships of basal neopterygians. In: Stiassny, M.L.J., Parenti, L.R., Johnson, G.D. (Eds.), Interrelationships of Fishes. Academic Press, San Diego, California, pp. 117–146. https://doi.org/10.1016/B978-012670950-6/50007-2
Gardiner, B.G., Schaeffer, B., 1989. Interrelationships of lower actinopterygian fishes. Zoological Journal of the Linnean Society. 1989, 135–187. https://doi.org/10.1111/j.1096-3642.1989.tb00550.x
Gardiner, B.G., Schaeffer, B., Masserie, J.A., 2005. A review of the lower actinopterygian phylogeny. Zoological Journal of the Linnean Society. 144, 511–525. https://doi.org/10.1111/j.1096-3642.2005.00181.x
Gegenbauer, C., 1887. Ueber die Occipitalregion und die ihr benachbarten Wirbel der Fische. In: Festschrift Albert von Kölliker Zur Feier Seines Siebenzigsten Geburtstages Gewidmet von Seinen Schülern. W. Engelmann, Leipzig.
Grande, L., 2010. An empirical synthetic pattern study of gars (Lepisosteiformes) and closely related species, based mostly on skeletal anatomy. The resurrection of Holostei., American Society of Ichthyologists and Herpetologists Special Publication 6:i–x, 1–871; supplementary issue of Copeia 10 (2A).
Grande, L., Bemis, W.E., 1991. Osteology and phylogenetic relationships of fossil and recent paddlefishes (Polyodontidae) with comments on the interrelationships of Acipenseriformes. Journal of Vertebrate Paleontology. 11, 1-121. https://doi.org/10.1080/02724634.1991.10011424
Grande, L., Bemis, W.E., 1998. A Comprehensive Phylogenetic Study of Amiid Fishes (Amiidae) Based on Comparative Skeletal Anatomy. an Empirical Search for Interconnected Patterns of Natural History. Journal of Vertebrate Paleontology. 18, 1–696. https://doi.org/10.1080/02724634.1998.10011114
Gregory, W.K.K., 1959. Fish skulls - A study of the evolution of natural mechanisms, Transactions of the American Philosophical Society. Eric Lundberg, Laurel, Florida.
Hammarberg, F., 1937. Zur Kenntnis der Ontogenetischen Entwicklung des Schädels von Lepisosteus platystomus. Acta Zoologica. 18, 210–336. https://doi.org/10.1111/j.1463-6395.1937.tb00680.x
Helfman, G., Collette, B., Facey, D., 2009. The diversity of fishes—biology, evolution, and ecology, 2nd edition. Wiley-Blackwell, Oxford, UK.
Hilton, E.J., Konstantinidis, P., Schnell, N.K., Dillman, C.B., 2014. Identity of a unique cartilage in the buccal cavity of gars (Neopterygii: Lepisosteiformes: Lepisosteidae). Copeia. 2014, 50–55. https://doi.org/10.1643/CI-12-173
Hilton, E.J., Schnell, N.K., Konstantinidis, P., 2015. When Tradition Meets Technology: Systematic Morphology of Fishes in the Early 21st Century. Copeia. 103, 858–873. https://doi.org/10.1643/CI-14-178
Ho, T.V., Iwata, J., Ho, H.A., Grimes, W.C., Park, S., Sanchez-Lara, P.A., Chai, Y., 2015. Integration of comprehensive 3D microCT and signaling analysis reveals differential regulatory mechanisms of craniofacial bone development. Developmental Biology. 400, 180–190. https://doi.org/10.1016/j.ydbio.2015.02.010
Hurley, I.A., Mueller, R.L., Dunn, K.A., Schmidt, E.J., Friedman, M., Ho, R.K., Prince, V.E., Yang, Z., Thomas, M.G., Coates, M.I., 2007. A new time-scale for ray-finned fish evolution. Proceedings. Biological sciences / The Royal Society. 274, 489–498. https://doi.org/10.1098/rspb.2006.3749
Huysseune, A., Sire, J.-Y., 1998. Evolution of patterns and processes in teeth and tooth-related tissues in non-mammalian vertebrates. European journal of oral sciences. 106, 437–481. https://doi.org/10.1111/j.1600-0722.1998.tb02211.x
Jessen, H., 1972. Schultergürtel und Pectoralflosse bei Actinopterygiern. Fossil Strata. 1, 1–101.
Jollie, M., 1984. Development of Cranial and Pectoral Girdle Bones of Lepisosteus with a Note on Scales. Copeia. 2, 476–502. https://doi.org/10.2307/1445204
Kammerer, C.F.F., Grande, L., Westneat, M.W.W., 2006. Comparative and Developmental Functional Morphology of the Jaws of Living and Fossil Gars (Actinopterygii : Lepisosteidae). Journal of morphology. 267, 1017–31. https://doi.org/10.1002/jmor.10293
Konstantinidis, P., Warth, P., Naumann, B., Metscher, B., Hilton, E.J., Olsson, L., 2015. The Developmental Pattern of the Musculature Associated with the Mandibular and Hyoid Arches in the Longnose Gar, Lepisosteus osseus (Actinopterygii, Ginglymodi, Lepisosteiformes). Copeia. 103, 920–932. https://doi.org/10.1643/OT-14-195
Kryzanovsky, S., 1927. Die Entwicklung der paarigen Flossen bei Acipenser, Amia und Lepidosteus. Acta Zoologica. 8, 278–352. https://doi.org/10.1111/j.1463-6395.1927.tb00654.x
Lauder, G. V., 1980. Evolution of the feeding mechanism in primitive actionopterygian fishes: A functional anatomical analysis of Polypterus, Lepisosteus, and Amia. Journal of Morphology. 163, 283–317. https://doi.org/10.1002/jmor.1051630305
Lebrun, R., 2014. ISE-MeshTools, a 3D interactive fossil reconstruction freeware. In: 12th Annual Meeting of EAVP, Torino, Italy.
Lecointre, G., Philippe, H., Van Le, H.L., Le Guyader, H., 1994. How many nucleotides are required to resolve a phylogenetic problem? The use of a new statistical method applicable to available sequences. Molecular Phylogenetics and Evolution. https://doi.org/10.1006/mpev.1994.1037
Long, J.M., Snow, R.A., 2016. Ontogenetic development of otoliths in alligator gar. Transactions of the American Fisheries Society. 145, 537–544. https://doi.org/10.1080/00028487.2015.1135189
Long, W.L., Ballard, W.W., 2001. Normal embryonic stages of the longnose gar, Lepisosteus osseus. BMC developmental biology. 1, 6. https://doi.org/10.1186/1471-213X-1-6
López-Arbarello, A., 2012. Phylogenetic Interrelationships of Gynglymodian Fishes (Actinopterygii: Neopterygii). PLoS ONE. 7, 1–44. https://doi.org/10.1371/journal.pone.0039370
Luther, A., 1913. Ueber die vom N. trigeminus versorgte Muskulatur der Ganoiden und Dipneusten. Helsingfors Acta Societas Scientiarum Fennica. 41, 1–72.
Maxwell, E.E., Wilson, L.A.B., 2013. Regionalization of the axial skeleton in the “ambush predator” guild -- are there developmental rules underlying body shape evolution in ray-finned fishes? BMC Evolutionary Biology. 13, 265. https://doi.org/10.1186/1471-2148-13-265
Mayhew, R.L., 1924. The skull of Lepidosteus platostomus. Journal of Morphology. 38, 315–346. https://doi.org/10.1002/jmor.1050380303
Metscher, B.D., 2009. MicroCT for developmental biology: A versatile tool for high-contrast 3D imaging at histological resolutions. Developmental Dynamics. 238, 632–640. https://doi.org/10.1002/dvdy.21857
Near, T.J., Eytan, R.I., Dornburg, A., Kuhn, K.L., Moore, J.A., Davis, M.P., Wainwright, P.C., Friedman, M., Smith, W.L., 2012. Resolution of ray-finned fish phylogeny and timing of diversification. Proceedings of the National Academy of Sciences. 109, 13698–13703. https://doi.org/10.1073/pnas.1206625109
Nelson, J.S., Grande, T.C., M. V. H. W, 2016. Order LEPISOSTEIFORMES - gars. In: Fishes of the World. John Wiley & Sons, New York.
Normark, B.B., McCune, a R., Harrison, R.G., 1991. Phylogenetic relationships of neopterygian fishes, inferred from mitochondrial DNA sequences. Molecular biology and evolution. 8, 819–834.
Palci, A., Lee, M.S.Y., Hutchinson, M.N., 2016. Patterns of postnatal ontogeny of the skull and lower jaw of snakes as revealed by micro-CT scan data and three-dimensional geometric morphometrics. Journal of Anatomy. https://doi.org/10.1111/joa.12509
Perry, S.F., Wilson, R.J. a, Straus, C., Harris, M.B., Remmers, J.E., 2001. Which came first, the lung or the breath? Comparative Biochemistry and Physiology - A Molecular and Integrative Physiology. 129, 37–47. https://doi.org/10.1016/S1095-6433(01)00304-X
Rice, R., Kallonen, A., Cebra-Thomas, J., Gilbert, S.F., 2016. Development of the turtle plastron, the order-defining skeletal structure. Proceedings of the National Academy of Sciences of the United States of America. 113, 5317–5322. https://doi.org/10.1073/pnas.1600958113
Rücklin, M., Donoghue, P.C.J., Cunningham, J.A., Marone, F., Stampanoni, M., 2014. Developmental Paleobiology of the Vertebrate Skeleton. Journal of Paleontology. 88, 676–683. https://doi.org/10.1666/13-107
Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., Tinevez, J.-Y., White, D.J., Hartenstein, V., Eliceiri, K., Tomancak, P., Cardona, A., 2012. Fiji: an open-source platform for biological-image analysis. Nature Methods. 9, 676–682. https://doi.org/10.1038/nmeth.2019
Schmalhausen, J.J., 1913. Zur Morphologie der unpaaren Flossen. II. Bau und Phylogenese der unpaaren Flossen und insbesonders der Schwanzflosse der Fische. Zeitschrift für wissenschaftliche Zoologie. 104, 1–80.
Schreiner, K.E., 1902. Einige Ergebnisse über den Bau und der Occipitalregion von Amia und Lepidosteus. Zetischriften. wiss. Zool. 72, 467–524.
Schultze, H.-P., Cloutier, R., 1991. Computed Tomography and Magnetic Resonance Imaging studies of Latimeria chalumnae. Environmental Biology of Fishes. 32, 159–181. https://doi.org/10.1007/BF00007451
Sewertzoff, A.N., 1895. Die Entwicklung der Occipitalregion der niederen Vertebraten im Zusammenhang mit der Frage nach der Metamerie des Kopfes. Bulletin de la société impériale des naturalistes de Moscou. 9, 186–284.
Shen, L., Ai, H., Liang, Y., Ren, X., Anthony, C.B., Goodlett, C.R., Ward, R., Zhou, F.C., 2013. Effect of prenatal alcohol exposure on bony craniofacial development: a mouse MicroCT study. Alcohol (Fayetteville, N.Y.). 47, 405–15. https://doi.org/10.1016/j.alcohol.2013.04.005
Sire, J.-Y., 1989. Scales in Young Polypterus senegalus Are Elasmoid : New Phylogenetic ImpIications. The American Journal of Anatomy. 186, 315–323. https://doi.org/10.1002/aja.1001860308
Sire, J.-Y., 1990. From ganoid to elasmoid scales in the actinopterygian fishes. Netherlands journal of zoology. 40, 75–92. https://doi.org/10.1163/156854289X00192
Sire, J.-Y., Donoghue, P.C.J., Vickaryous, M.K., 2009. Origin and evolution of the integumentary skeleton in non-tetrapod vertebrates. Journal of Anatomy. 214, 409–440. https://doi.org/10.1111/j.1469-7580.2009.01046.x
Sire, J.-Y., Géraudie, J., Meunier, F.J., Zylberberg, L., 1987. On the Origin of Ganoine: Histological and Ultrastructural Data on the Experimental Regeneration of the Scales of Calamoichthys calabaricus (Osteichthyes, Brachyopterygii, Polypteridae). The American Journal of Anatomy. 180, 391–402. https://doi.org/10.1002/aja.1001800409
Slater, B.J., Liu, K.J., Kwan, M.D., Quarto, N., Longaker, M.T., 2009. Cranial osteogenesis and suture morphology in Xenopus laevis: A unique model system for studying craniofacial development. PLoS ONE. 4. https://doi.org/10.1371/journal.pone.0003914
Veit, O., 1907. Über einige Besonderheiten am Primordialcranium von Lepidosteus osseus. Anatomische Hefte. 99, 155–204. https://doi.org/10.1007/BF02214184
Vickaryous, M.K., Sire, J.Y., 2009. The integumentary skeleton of tetrapods: Origin, evolution, and development. Journal of Anatomy. 214, 441–464. https://doi.org/10.1111/j.1469-7580.2008.01043.x
Wiley, E.O., 1976. The phylogeny and biogeography of fossil and recent gars (Actinopterygii: Lepisosteidae). University of Kansas Museum of Natural History Miscellaneous Publications. 64, 1–111.
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