Skip to main content
SpringerLink
Log in

Role of the neural crest in development of the cartilaginous cranial and visceral skeleton of the medaka, Oryzias latipes (Teleostei)

  • Published:
Anatomy and Embryology Aims and scope Submit manuscript

Summary

Neural crestectomies were performed on neurula stage medaka embryos to remove neural crest with tungsten needles from one of five anteriorly located zones. The embryos were allowed to develop to stage 35 (immediately posthatching) larvae, then cleared and stained for cartilage. An analysis of changes to the head skeletons indicated that most of the anterior neurocranium and the entire viscerocranium received neural crest contributions during development. The elements involved included; the lamina orbitonasalis of the nasal capsule, the trabeculae, Meckels' cartilage and the quadrate of the lower jaw, the pterygoid process, the orbital cartilages and the epiphyseals of the neurocranial roof, as well as all the elements of the hyoid and branchial arches. By further analysis of only those neural crest ablations which produced alterations to the head skeleton, the neural crest cells which contributed to the development of each element were mapped. They originated principally, from one of three regions; the mesencephalon (second most anterior zone removed, number II), the preotic rhombencephalon (zone III), or the postotic rhombencephalon (zone IV). Neural crest from the level of the prosencephalon (zone I) was not chondrogenic nor was neural crest from the fifth region (zone V) which extended beyond the 5th to about the 8th or 10th somite and marked the anterior end of trunk neural crest. The data are discussed and are found to be consistent with the results from other vertebrates and support the central role of the neural crest in the development and evolution of the vertebrate bead skeleton.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Bodenstein D (1952) Studies on the development of the dorsal fin in Amphibians. J Exp Zool 120:213–245

    Google Scholar 

  • Bronner-Fraser M (1982) Distribution of latex beads and retinal pigment cells along the ventral neural crest pathway. Dev Biol 91:50–63

    Google Scholar 

  • Bronner-Fraser M (1984) Latex beads with defined surface coats as probes of neural crest pathways. In: Trelstad RL (ed) The role of extracellular matrix in development, Alan R. Liss Inc, New York, pp 399–432

    Google Scholar 

  • Chibon P (1966) Analyse expérimentale de la régionalisation et des capacités morphogénétics de la crêtes neurales chez l'amphibien Urodèle Pleurodeles waltilii Michah. Mem Soc Fr Zool 36:1–107

    Google Scholar 

  • Chibon P (1967) Marquage nucléaire par la thymidine tritée des dérivés de la crête neurale chez l'amphibien urodèle Pleurodeles waltlii Michah. J Embryol Exp Morphol 18:343–358

    Google Scholar 

  • deBeer GR (1937) The development of the vertebrate skull. Oxford University Press, Oxford. Reprinted 1985, Chicago Univ Press, Chicago

    Google Scholar 

  • Fluck R, Gunning R, Pelegrino J, Barron T, Panitch D (1983) Rhythmic contractions of the blastoderm of the medaka, Oryzias latipes, a teleost. J Exp Zool 226:245–253

    Google Scholar 

  • Gamo H, Terajima I (1963) The normal stages of embryonic development of the medaka, Oryzias latipes. Jap J Ichthyol 10:31–37

    Google Scholar 

  • Gans C, Northcutt RG (1983) Neural crest and the orgin of vertebrates: a new head. Science 220:268–274

    Google Scholar 

  • Hall BK (1978) Developmental and cellular skeletal biology. Academic Press, New York

    Google Scholar 

  • Hall BK (1980) Chondrogenesis and osteogenesis of neural crest cells. In: Pratt RM, Christiansen RL (eds) Current trends in prenatal craniofacial development. Elsevier North-Holland, New York, pp 47–63

    Google Scholar 

  • Hall BK (1983) Epigenetic control in development and evolution. In: Goodwin BC, Holder N, Wylie CC (eds) Development and Evolution. Sixth Symposium of the British Society for Developmental Biology. Cambridge University Press, Cambridge, pp 353–380

    Google Scholar 

  • Hall BK (1984) Genetic and epigenetic control of connective tissues in the craniofacial structures. In: Brown KS, Salinas CF (eds) Craniofacial Mesenchyme in Morphogenesis and Malformation. Proceedings of the Sixth Annual Symposium of the Society of Craniofacial Genetics Held in Seattle, Washington, June 19, 1983. Birth Defects: Original Article Series, Vol 20, No 3. Alan R. Liss, New York, pp 1–18

    Google Scholar 

  • Hall BK (1987a) Tissue interactions in the development and evolution of the vertebrate head. In: Maderson PFA (ed) Development and evolution of the neural crest. J Wiley and Sons, London (in press)

    Google Scholar 

  • Hall BK (1987b) Earliest evidence of cartilage and bone development in embryonic life. Clin Orthop (in press)

  • Hardisty MW (1981) The skeleton. In: Hardisty MW, Potter JC (eds) The biology of lampreys, vol 3, Academic Press, New York, pp 333–376

    Google Scholar 

  • Hörstadius S (1950) The neural crest its properties and derivatives in light of experimental research. Oxford University Press, Oxford

    Google Scholar 

  • Johnston MC (1966) A radioautographic study of the migration and fate of cranial neural crest cells in the chick embryo. Anat Rec 156:143–156

    Google Scholar 

  • Kelly WL, Bryden MM (1983) A modified differential stain for cartilage and bone in whole mount preparations of mammalian fetuses and small vertebrates. Stain Technol 58:131–134

    Google Scholar 

  • Lamers CH, Rombout JWHM, Timmermans LPM (1981) An experimental study on neural crest migration in Barbus conchions (Cyprinidae, Teleostei), with special reference to the origin of the enteroendocrine cells. J Embryol Exp Morphol 62:309–323

    Google Scholar 

  • Langille RM, Hall BK (1986) Evidence of cranial neural crest contribution to the skeleton of the sea lamprey Petromyzon marinus. In: Slavkin H (ed) Progress in developmental biology, Pt2, Alan R Liss, New York, pp 263–266

    Google Scholar 

  • Langille RM, Hall BK (1987a) Development of the head skeleton of the japanese medaka, Oryzias latipes (Teleostei). J Morphol 193:135–158

    Google Scholar 

  • Langille RM, Hall BK (1987b) Role of the neural crest in development of the trabeculae and branchial arches in embryonic sea lamprey, Petromyzon marinus (L.). Development (in press)

  • Le Douarin NM (1982) The neural crest. Cambridge University Press, Cambridge

    Google Scholar 

  • Le Lièvre C (1971a) Recherches sur l'origine embryologique des arcs viscéraux chez l'embryon d'Oiseau par la methode des greffes interspécifiques entre Caille et Poulet. CR Soc Biol 165:395–400

    Google Scholar 

  • Le Lièvre C (1971b) Recherches sur l'origine embryologique du squelette viscéral chez l'embryon d'Oiseau. CR Assoc Anat 152:575–583

    Google Scholar 

  • Le Lièvre C (1974) Rôle des cellules mésectodermiques issues des crêtes neurales céphaliques dans la formation des arcs branchiaux et du squelette viscéral. J Embryol Exp Morphol 31:453–477

    Google Scholar 

  • Le Lièvre C (1978) Participation of neural crest derived cells in the genesis of the skull in birds. J Embryol Exp Morphol 47:17–37

    Google Scholar 

  • Le Lièvre C, LeDouarin NM (1975) Mesenchymal derivatives of the neural crest: analysis of chimaeric quail and chick embryos. J Embryol Exp Morphol 34:125–154

    Google Scholar 

  • Lehman F, Youngs LM (1952) An analysis of regulation in the amphibian neural crest. J Exp Zool 121:419

    Google Scholar 

  • Lopashov GV (1944) Origin of pigment cells and visceral cartilage in teleosts. CR Acad Sci USSR 4:169–172

    Google Scholar 

  • McKee GJ, Ferguson NWJ (1984) The effects of mesencephalic neural crest cell extirpation on the development of chicken embryos. J Anat 139:491–512

    Google Scholar 

  • Newth DR (1956) On the neural crest of lamprey embryos. J Embryol Exp Morphol 4:358–375

    Google Scholar 

  • Niu MC (1954) Further studies on the origin of amphibian pigment cells. J Exp Zool 125:199–220

    Google Scholar 

  • Noden DM (1975) An analysis of the migratory behavior of avian cephalic neural crest cells. Dev Biol 42:106–130

    Google Scholar 

  • Noden DM (1978) Interactions directing the migration and cytodifferentiation of avian neural crest cells. In: Garrod D (ed) The specificity of embryological interactions, Chapman Hall, London, pp 4–49

    Google Scholar 

  • Noden DM (1983) The role of the neural crest in patterning of avian cranial skeletal, connective, and muscle tissues. Dev Biol 96:144–165

    Google Scholar 

  • Northcutt RG, Gans C (1983) The genesis of neural crest and epidermal placodes: a reinterpretation of vertebrate origins. Quart Rev Biol 58:1–28

    Google Scholar 

  • Orton GL (1953) Development and migration of pigment cells in some teleost fishes. J Morphol 93:69–99

    Google Scholar 

  • Rosen DE, Parenti LR (1981) Relationships of Oryzias and the groups of atherinomorph fishes. Am Mus Natl His Novitates 2719:1–25

    Google Scholar 

  • Toerien MJ (1965) Experimental studies on the columella-capsular interrelationships in the turtle, Chelydra serentina. J Embryol Exp Morphol 14:265–272

    Google Scholar 

  • Twitty VC (1949) Developmental analysis of amphibian pigmentation. Growth Symp 9:133–161

    Google Scholar 

  • Weston JA (1970) The migration and differentiation of neural crest cells. Adv Morphogenesis 8:41–114

    Google Scholar 

  • Yamamoto T (1975) Medaka (killifish): biology and strains. Keigaku Publ, Tokyo

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biology, Dalhousie University, B3H 4J1, Halifax, Nova Scotia, Canada

    Robert M. Langille & Brian K. Hall

Authors
  1. Robert M. Langille
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Brian K. Hall
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Langille, R.M., Hall, B.K. Role of the neural crest in development of the cartilaginous cranial and visceral skeleton of the medaka, Oryzias latipes (Teleostei). Anat Embryol 177, 297–305 (1988). https://doi.org/10.1007/BF00315836

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00315836

Key words

Search

Navigation