Neural crest contribution to the avian shoulder girdle and implications to girdle evolution in vertebrates
DOI:
https://doi.org/10.21638/11701/spbu03.2017.104Abstract
Neural crest (NC) is an established source for many endochondral and intramembranous bones in the skull and postcranial skeleton in vertebrates. Neural crest cells also contribute to the trapezius/cleidohyoideus muscle attachment sites on the shoulder girdle of the mouse, where they are found in the scapula, clavicle, and sternum. In the avian shoulder girdle, NC cells from the level of the first two cranial−most somites were only found so far in the clavicle, while in the axolotl, the NC contribution to the shoulder girdle was not found at all. In this study we aimed to determine whether NC cells caudal to the level of the second somite contribute to the cartilaginous shoulder girdle in birds and to analyse the phylogenetic distribution of NC cells in the vertebrate shoulder girdle. Homotopic quail to chick embryos and GFP+ to white chick embryos transplantations of the neural tube including presumptive NC, as well as immunohistochemical detection of NC markers, such as HNK-1 and PDGFRα revealed no contribution of NC cells from somite levels 3−27 to the skeletal elements of the shoulder girdle, including, but not restricting to muscle attachment sites, despite abundance of other NC derivatives. Thus, in birds, NC does not contribute to the formation of the cartilaginous shoulder girdle. The negative result is discussed in a broad evolutionary aspect. It supports the notion of the uniqueness of NC contribution to the variety of endochondral bones in mice (or mammals). In other vertebrates, including birds, only the cells of the cranial NC seem to migrate to the shoulder girdle and contribute to the intramembranous clavicles and/or interclavicle. We critically evaluate the existing hypotheses on evolution of NC contribution to the shoulder girdle in vertebrates.
Keywords:
neural crest, shoulder girdle, clavicle, scapula, evolution, chick, vertebrates, chimeras, HNK-1, PDGFRα
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References
Barriga, E. H., Trainor, P. A., Bronner, M., and Mayor, R. 2015. Animal models for studying neural crest development: is the mouse different? Development 142:1555–1560.
Bronner-Fraser, M. 1986. Analysis of the early stages of trunk neural crest migration in avian embryos using monoclonal antibody HNK-1. Developmental Biology 115 (1):44–55.
Broom, R. 1900. XXIX. — On the development and morphology of the marsupial shoulder girdle. Earth and Environmental Science Transactions of the Royal Society of Edinburgh 39 (03):749–770.
Cebra-Thomas, J. A., Betters, E., Yin, M., Plafkin, C., McDow, K., and Gilbert, S. F. 2007. Evidence that a late-emerging population of trunk neural crest cells forms the plastron bones in the turtle Trachemys scripta. Evolution and Development 9:267–277.
Chai, Y., Jiang, X., Ito, Y., Bringas, P., Han, J., Rowitch, D. H., Soriano, P., McMahon, A. P., and Sucov, H. M. 2000. Fate of the mammalian cranial neural crest during tooth and mandibular morphogenesis. Development 127 (8):1671–1679.
Cherepanov, G. O. 1997. The origin of the bony shell of turtles as a unique evolutionary model in reptiles. Russian Journal of Herpetology 4:155–162.
Chevallier, A. 1977. Origine des ceintures scapulaires et pelviennes chez l’embryon d’oiseau. Journal of Embryology and Experimental Morphology 42:275–292.
Clark, K., Bender, G., Murray, B. P., Panfilio, K., Cook, S., Davis, R., Murnen, K., Tuan, R. S., and Gilbert, S. F. 2001. Evidence for the neural crest origin of turtle plastron bones. Genesis 31:111–117.
Coates, M. I. 1994. The origin of vertebrate limbs. Development Suppl.: 169–180.
Coates, M. I., Ruta, M., and Friedmann, M. 2008. Ever since Owen: Changing perspectives on the early evolution of tetrapods. Annual Review of Ecology, Evolution, and Systematics 39:571–592.
Davidian, A. and Malashichev, Y. 2013. Dual embryonic origin of the hyobranchial apparatus in Mexican axolotl (Ambystoma mexicanum). International Journal of Developmental Biology 57 (11/12).
Epperlein, H.-H., Khattak, S., Knapp, D., Tanaka, E. M., and Malashichev, Y. 2012. Neural crest does not contribute to the neck and shoulder in the Axolotl (Ambystoma mexicanum). PLoS ONE 7 (12):e52244.
Gans, C. and Northcut, R. G. 1983. Neural crest and the origin of vertebrates: the new head. Science 220:268–273.
Gilbert, S. F., Bender, G., Betters, E., Yin, M., and Cebra-Thomas, J. A. 2007. The contribution of neural crest cells to the nuchal bone and plastron of the turtle shell. Integrative and Comparative Biology 47:401–408.
Grandel, H. and Schulte-Merker, S. 1998. The development of the paired fins in the Zebrafish (Danio rerio). Mechanisms of Development 79:99–120.
Gross, J. B. and Hanken, J. 2008. Review of fate-mapping studies of osteogenic cranial neural crest in vertebrates. Developmental Biology 317:389–400.
Hall, B. K. and Gillis, J. A. 2013. Incremental evolution of the neural crest, neural crest cells and neural crest-derived skeletal tissues. Journal of Anatomy 222 (1):19–31.
Hamburger, V. and Hamilton, H. L. 1951. A series of normal stages in the development of the chick embryo. Journal of Morphology 88:49–92.
Heatwole, H. and Carroll, R. L. 2000. Amphibian Biology. Vol. 4. Palaeontology: The Evolutionary History of Amphibians, edited by H. Heatwole. Chipping Norton, Australia: Surrey Beatty & Sons.
Ho, L., Symes, K., Yordán, C., Gudas, L. J., and Mercola, M. 1994. Localization of PDGF A and PDGFR alpha mRNA in Xenopus embryos suggests signalling from neural ectoderm and pharyngeal endoderm to neural crest cells. Mechanisms of Development 48 (3):165–174.
Johanson, Z., Joss, J. M. P., and Wood, D. 2004. The scapulocoracoid of the Quensland lungfish Neoceratodus forsteri (Dipnoi: Sarcopterygii): morphology, development and evolutionary implications for bony fishes (Osteichthyes). Zoology 107:93–109.
Joyce, W. G., Jenkins, F. A., and Rowe, T. 2006. The presence of cleithra in the basal turtle Kayentachelis aprix. Russian Journal of Herpetology 13 (Suppl.):104–111.
Kague, E., Gallagher, M., Burke, S., Parsons, M., Franz-Odendaal, T., and Fischer, S. 2012. Skeletogenic fate of zebrafish cranial and trunk neural crest. PLoS ONE 7 (11):e47394.
Klima, M. 1973. Die Fruhentwicklung des Schurtelgurtels und des Brustbeins den Monotremen (Mammalia: Prototheria). Advances in Anatomy, Embryology, and Cell Biology 47:1–80.
Lebedev, O. A. and Coates, M. I. 2008. The postcranial skeleton of the Devonian tetrapod Tulerpeton curtum Lebedev. Zoological Journal of Linnean Society, London 114 (3):307–348.
Lyson, T. R., Bhullar, B.-A. S., Bever, G. S., Joyce, W. G., de Queiroz, K., Abzhanov, A., and Gauthier, J. A. 2013. Homology of the enigmatic nuchal bone reveals novel reorganization of the shoulder girdle in the evolution of the turtle shell. Evolution and Development 15 (5):317–325.
Matsuoka, T., Ahlberg, P. E., Kessaris, N., Iannarelli, P., Dennehy, U., Richardson, W. D., McMahon, A. P., and Koentges, G. 2005. Neural crest origins of the neck and shoulder. Nature 436:347–355.
McGonnell, I. 2001. The evolution of the pectoral girdle. Journal of Anatomy 199:189–194.
McGonnell, I. and Graham, A. 2002. Trunk neural crest has skeletogenic potential. Current Biology 12:767–771.
McGonnell, I. M., McKay, I. J., and Graham, A. 2001. A population of caudally migrating cranial neural crest cells: functional and evolutionary implications. Developmental Biology 236:354–363.
McGrew, M., Sherman, A., Ellard, F., Lillico, S., Gilhooley, H., Kingsman, A., Mitrophanous, K., and Sang, H. 2004. Efficient production of germline transgenic chickens using lentiviral vectors. EMBO Reports 5 (7):728–733.
Mongera, A., Singh, A. P., Levesque, M. P., Chen, Y.-Y., Konstantinidis, P., and Nüsslein-Volhard, C. 2013. Genetic lineage labeling in zebrafish uncovers novel neural crest contributions to the head, including gill pillar cells. Development 140:916–925.
Murdoch, B., DelConte, C., and García-Castro, M. I. 2012. Pax7 lineage contributions to the mammalian neural crest. PLoS ONE 7 (7):e41089.
Nagashima, H., Fumiaki, S., Tekechi, M., Sato, N., and Kuratani, S. 2014. On the homology of the shoulder girdle in turtles. Journal of Experimental Zoology (Molecular Development and Evolution) 324B:244–254.
Nagashima, H., Shibata, M., Taniguchi, M., Ueno, S., Kamezaki, N., and Sato, N. 2014. Comparative study of the shell development of hardand soft-shelled turtles. Journal of Anatomy 225 (1):60–70.
Nakamura, H. and Ayer-le Lievre, C. S. 1982. Mesectodermal capabilities of the trunk neural crest of birds. Journal of Embryology and Experimental Morphology 70:1–18.
Parker, W. K. 1868. A monograph on the structure and development of the shoulder-girdle and sternum in the Vertebrata. London: Ray Society.
Rickmann, M., Fawcett, J. W., and Keynes, R. J. 1985. The migration of neural crest cells and the growth of motor axons through the rostral half of the chick somite. Journal of Embryology and Experimental Morphology 90:437–455.
Sanchez-Villagra, M. R. and Maier, W. 2003. Ontogenesis of the scapula in marsupial mammals, with special emphasis on perinatal stages of didelphids and remarks on the origin of the therian scapula. Journal of Morphology 258:115–129.
Sánchez-Villagra, M. R. and Maier, W. 2006. Homologies of the mammalian shoulder girdle: a response to Matsuoka et al. (2005). Evolution and Development 8:113–115.
Schatteman, G. C., Morrison-Graham, K., van Koppen, A., Weston, J. A., and Bowen-Pope, D. F. 1992. Regulation and role of PDGF receptor alpha-subunit expression during embryogenesis. Development 115 (1):123–131.
Schilling, T. F. and Kimmel, C. B. 1994. Segment and cell type lineage restrictions during pharyngeal arch development in the zebrafish embryo. Development 120:483–494.
Schneider, R. A. 1999. Neural crest can form cartilages normally derived from mesoderm during development of the avian head skeleton. Developmental Biology 208:441–455.
Theis, S. 2010. Origin and development of the cucullaris/trapezius-sternocleidomastoid muscles in birds, mammals and reptiles, Department of Anatomy and Cell Biology, Albert-Lüdwigs-Universität Freiburg im Breisgau, Freiburg im Breisgau.
Theis, S., Patel, K., Valasek, P., Otto, A., Pu, Q., Harel, I., Tzahor, E., Tajbakhsh, S., Christ, B., and Huang, R. 2010. The occipital lateral plate mesoderm is a novel source for vertebrate neck musculature. Development 137:2961–2971.
Tschopp, E. and Mateus, O. 2013. Clavicles, interclavicles, gastralia, and sternal ribs in sauropod dinosaurs: new reports from Diplodocidae and their morphological, functional and evolutionary implications. Journal of Anatomy 222:321–340.
Tucker, G. C., Lipinski, M., Tursz, T., and Thiery, J.-P. 1984. Identical reactivity of monoclonal antibodies HNK-1 and NC-1: conservation in vertebrates on cells derived from the neural primordium and on some leukocytes. Cell Differentiation 14:223–230.
Valasek, P., Theis, S., Krejci, E., Grim, M., Maina, F., Schwartz, Y., Otto, A., Huang, R., and Patel, K. 2010. Somitic origin of the medial border of the mammalian scapula and its homology to the avian scapula blade. Journal of Anatomy 216:482–488.
Vallen, E. 1942. Beiträge zur Kenntnis der Ontogenie und der vergleichenden Anatomie des Schildkrötenpanzers. Acta Zoologica 23 (1/3):1–127.
Vickaryous, M. K. and Hall, B. K. 2006. Homology of the reptilian coracoid and a reappraisal of the evolution and development of the amniote pectoral apparatus. Journal of Anatomy 208:263–285.
Vickaryous, M. K. and Hall, B. K. 2010. Comparative development of the crocodylian interclavicle and avian furcula, with comments on the homology of dermal elements in the pectoral apparatus. Journal of Experimental Zoology (Molecular Development and Evolution) 314B:196–207.
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Published
2017-04-01
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Ponomartsev, S., Valasek, P., Patel, K., & Malashichev, Y. (2017). Neural crest contribution to the avian shoulder girdle and implications to girdle evolution in vertebrates. Biological Communications, 62(1), 26–37. https://doi.org/10.21638/11701/spbu03.2017.104
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