Skip to main content
Log in

Evolutionary developmental biology and vertebrate head segmentation: A perspective from developmental constraint

  • Published:
Theory in Biosciences Aims and scope Submit manuscript

Summary

The question of vertebrate head segmentation has become one of the central issues in Evolutionary Developmental Biology. Beginning as a theory based in comparative anatomy, a segmental theory of the head has been adopted and further developed by comparative embryologists. With the use of molecular and cellular biology, and in particular analyses of the Hox gene complex, the question has been addressed at new levels, but it remains unresolved. In this review, vertebrate head segmentation is reevaluated, by introducing findings from experimental embryology and evolutionary biology. Developmental biology has shown that pattern is generated through hierarchically organized and causally linked series of events. The question of head segmentation can be viewed as a question of generative constraint, that is whether segmentation in the head is imposed by underlying segmental patterns, as it is in the trunk. In this respect, amphioxus appears to be segmented along the entire anteroposterior axis, with myotomes and peripheral nerves repeating with the same rhythm (somitomerism). Similarly, in the vertebrate trunk, the segmental patterns shared by myotomes, peripheral nerves and vertebrae are derived from the somites. However, in the head of vertebrates there is no such mesodermal pattern, although neuromerism and branchiomerism do indicate the presence of constraints derived from rhombomeres and pharyngeal pouches, respectively. These data fit better the concept of dual metamerism of the vertebrate body proposed by Romer (1972), than the traditional head cavity-based segmental model by Goodrich (1930).

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Adelmann, H. B. (1925) The development of the neural folds and cranial ganglia of the rat. J. Comp. Neurol. 39: 19–171.

    Article  Google Scholar 

  • Adelmann, H. B. (1927) The development of the eye muscles of the chick. J. Morphol. Physiol. 44: 29–87.

    Article  Google Scholar 

  • Ahlborn, F. (1884) Ueber die Segmentation des Wirbelthierkörpers. Z. wiss. Zool. 40: 309–337.

    Google Scholar 

  • Anderson, C. B., Meier, S. (1981). The influence of the metameric pattern in the mesoderm on migration of cranial neural crest cells in the chick embryo. Dev. Biol. 85: 385–402.

    Article  PubMed  CAS  Google Scholar 

  • Balfour, F. M. (1878) The development of the elasmobranchial fishes. J. Anat. Physiol. 11: 405–706.

    Google Scholar 

  • de Beer, G. R. (1922). The segmentation of the head in Squalus acanthias. Quart, J. microsc. Sci. 66: 4578–474.

    Google Scholar 

  • de Beer, G. R. (1937) The Development of the Vertebrate Skull, Oxford University Press, London.

    Google Scholar 

  • Begbie, J., Brunet, J. F., Rubenstein, J. L., Graham, A. (1999) Induction of the epibranchial placodes. Development 126: 895–902.

    PubMed  CAS  Google Scholar 

  • Bjerring, H. C. (1977) A contribution to structual analysis of the head of craniate animals. Zool. Scripta 6: 127–183.

    Google Scholar 

  • Bowler, P. J. (1996) Life’s Splendid Drama, Univ. Chicago Press, Chicago & London.

    Google Scholar 

  • Brachet, A. (1935). Traié d’Embryologie des Vertébrés, Masson & Cie, Etiteurs, Paris.

    Google Scholar 

  • Bronner-Fraser, M. (1986) Analysis of the early stages of trunk neural crest cell migration in avian embryos using monoclonal antibody, HNK-1. Dev. Biol. 115: 44–55.

    Article  PubMed  CAS  Google Scholar 

  • Chambers, D., Mason, I. (2000) Expression of sprouty2 during early development of the chick embryo is coincident with known sites of FGF signalling. Mech Dev. 91: 361–364.

    Article  PubMed  CAS  Google Scholar 

  • Couly, G. F., Colty, P. M., Le Douarin, N. M. (1992) The developmental fate of the cephalic mesoderm in quail - chick chimeras. Development 114: 1–15.

    PubMed  CAS  Google Scholar 

  • Damas, H. (1944) Recherches sur le développement de Lampetra fluviatilis L. - contribution à l’étude de la cephalogénèse des vertébrés. Arch. Biol., Paris 55: 1–289.

    Google Scholar 

  • Dean, B. (1899) On the embryology of Bdellostoma stouti. A genera account of myxinoid development from the egg and segmentation to hatching. Festschrift zum 70ten Geburtsstag Carl von Kupffer, Jena, pp 220–276.

    Google Scholar 

  • Detwiler, S. R. (1934) An experimental study of spinal nerve segmentation in Amblystoma with reference to the plurisegmental contribution to the brachial plexus. J. Exp. Zool. 67: 395–441.

    Article  Google Scholar 

  • Dohrn, A. (1890) Bemerkungen über den neuesten Versuch einer Lösung des Wirbelthierkopf-Problems. Anat. Anz. 5: 53–64, 78–85.

    Google Scholar 

  • Figdor, M. C., Stern, C. D. (1993) Segmental organization of embryonic diencephalon. Nature 363: 630–634.

    Article  PubMed  CAS  Google Scholar 

  • Fraser, E. A. (1915) The head cavities and development of the eye muscles in Trichosurus vulpecula, with notes on some other marsupials. Proc. Zool. Soc. 22: 299–346.

    Google Scholar 

  • Fraser, S., Keynes, R., Lumsden, A. (1990) Segmentation in the chick embryo hindbrain is defined by cell lineage restriction. Nature 344: 431–435.

    Article  PubMed  CAS  Google Scholar 

  • Freund, R., Dörfler, D., Popp, W., Wachtler, F. (1996) The metameric pattern of the head mesoderm — does it exist? Anat. Embryol. 193: 73–80.

    Article  PubMed  CAS  Google Scholar 

  • Fritzsch, B., Northcutt, G. (1993) Cranial and spinal nerve organization in Amphioxus and Lampreys: evidence for an ancestral craniate pattern. Act. anat. 148: 96–109.

    Article  CAS  Google Scholar 

  • Froriep, A. (1885) Über Anlagen von Sinnesorganen am Facialis, Glossopharyngeus und Vagus, über die genetische Stellung des Vagus zum Hypoglossus, und über die Herkunft der Zungenmusculatur. Arch. Anat. Physiol. 1885: 1–55.

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Garel, S., Garcia-Dominguez, M., Charnay, P. (2000) Control of the migratory pathway of facial branchiomotor neurones. Development 127: 5297–5307.

    PubMed  CAS  Google Scholar 

  • Gaupp, E. (1898) Die Metamerie des Schädels. Erg. Anat. Ent.-ges. 7: 793–885.

    Google Scholar 

  • Gee, H. (1996) Before the Backbone, Chapman & Hall, London.

    Google Scholar 

  • Gegenbaur, C. (1888) Die Metamerie des Kopfes. Morph. Jb. 13: 1–114.

    Google Scholar 

  • Gegenbaur, C. (1898) Vergleichende Anatomie der Wirbelthiere mit Berücksichtigung der Wirbellosen. Leipzig: Verlag von Wilhelm Engelmann.

    Google Scholar 

  • Gendron-Maguire, M., Mallo, M., Zhang, M., Gridley, T. (1993) Hoxa-2 mutant mice ehibit homeotic transformation of skeletal elements derived from cranial neural crest. Cell 75: 1317–1331.

    Article  PubMed  CAS  Google Scholar 

  • Grammatopoulos, G. A., Bell, E., Toole, L., Lumsden, A., Tucker, A. S. (2000) Homeotic transformation of branchial arch identity after Hoxa2 overexpression. Development 127: 5355–5365.

    PubMed  CAS  Google Scholar 

  • Goethe, J. W. (1790) Das Schädelgrüt aus sechs Wirbelknochen aufgebaut. Zur Naturwissenschaft überhaupt, besonders zur Morphologie. II 2 (cited in Gaupp 1898).

  • Goethe, J. W. (1820) Zur Naturwissenschaft überhaupt, besonders zur Morphologie. I, J. G. Cotta, Stuttgart & Tübingen.

    Google Scholar 

  • Goodrich, E. S. (1918) On the development of the segments of the head in Scyllium. Quart. J. microsc. Sci. 63: 1–30.

    Google Scholar 

  • Goodrich, E. S. (1930) Structure and Development of Vertebrates, Macmillan, London.

    Google Scholar 

  • Goronowitsch, N. (1892) Die axiale und die laterale (A. Goette) Kopfmetamerie der Vögelembryonen. Die Rolle der sogenatte ‚Ganglienleisten‘ im Aufbaue der Nervenstamme. Anat. Anz. 7: 454–464.

    Google Scholar 

  • Graham, A., Heyman, I., Lumsden, A. (1993) Even-numbered rhombomeres control the apoptotic elimination of neural crest cells from odd-numbered rhombomeres in the chick hindbrain. Development 119: 233–245.

    PubMed  CAS  Google Scholar 

  • Graham, A. (2001) The development and evolution of the pharyngeal arches. J. Anat. 199: 133–141.

    Article  PubMed  CAS  Google Scholar 

  • Guthrie, S., Muchamore, I., Kuroiwa, A., Marshall, H., Krumlauf, R., Lumsden, A. (1992) Neuroectodermal autonomy of Hox-2.9 expression revealed by rhombomere transpositions. Nature 356: 157–159.

    Article  PubMed  CAS  Google Scholar 

  • Hall, B. K. (1998) Evolutionary Developmental Biology. 2nd ed., Chapman & Hall, London.

    Google Scholar 

  • Hertwig, O. (1906) Handbuch der vergleichenden und experimentellen Entwicklungslehre der Wirbelthiere, Gustav Fischer, Jena.

    Google Scholar 

  • Hill, C. (1900) Developmental history of primary segments of the vertebrate head. Zool. Jb. 13: 393–446.

    Google Scholar 

  • Hoffmann, C. K. (1897) Betraege zur Entwicklung der Selachier. Morphol. Jb. 25: 250–304.

    Google Scholar 

  • Holland, P. W. (2000) Embryonic development of heads, skeletons and amphioxus: Edwin S. Goodrich revisited. Int. J. Dev. Biol. 44: 29–34.

    PubMed  CAS  Google Scholar 

  • Horigome, N., Myojin, M., Hirano, S., Ueki, T., Aizawa, S., Kuratani, S. (1999) Development of cephalic neural crest cells in embryos of Lampetra japonica, with special reference to the evolution of the jaw. Dev. Biol. 207: 287–308.

    Article  PubMed  CAS  Google Scholar 

  • Hughes, C. L., Kaufman, T. C. (2002) Hox genes and the evolution of the arthropod body plan. Evol. Dev. 4: 459–499.

    Article  PubMed  CAS  Google Scholar 

  • Hunt, P., Krumlauf, R. (1991) Deciphering the Hox code: clues to patterning branchial regions of the head. Cell 66: 1075–1078.

    Article  PubMed  CAS  Google Scholar 

  • Hunt, P., Gulisano, M., Cook, M., Sham, M.-H., Faiella, A., Wilkinson, D., Boncinelli, E., Krumlauf, R. (1991) A distinct Hox code for the branchial region of the vertebrate head. Nature 353: 861–864.

    Article  PubMed  CAS  Google Scholar 

  • Huxley, T. H. (1858) The Croonian Lecture. — On the theory of the vertebrate skull. Proc. Zool. Soc. London, 9: 381–457.

    Article  Google Scholar 

  • Inoue, T., Chisaka, O., Matsunami, H., Takeichi, M. (1997) Cadherin-6 expression transiently delineates specific rhombomeres, other neural tube subdivisions, and neural crest subpopulations in mouse embryos. Dev. Biol. 183: 183–194.

    Article  PubMed  CAS  Google Scholar 

  • Jacob, M., Jacob, H. J., Wachtler, F., Christ, B. (1984) Ontogeny of avian extrinsic ocular muscles. I. A light- and electron-microscopic study. Cell Tiss. Res. 237: 549–557.

    Article  CAS  Google Scholar 

  • Jacobson, A. G. (1988) Somitomeres: mesodermal segments of vertebrate embryos. Development 104 suppl. 1988: 209–220.

    Google Scholar 

  • Jacobson, A. G. (1993) Somitomeres: Mesodermal segments in the head and trunk. In: Hanken, J., Hall, B. K. (eds) The Vertebrate Skull Vol. 1. Chicago: University of Chicago Press, pp 42–76.

    Google Scholar 

  • Jarvik, E. (1980) Basic Structure and Evolution of Vertebrates, Academic Press, London.

    Google Scholar 

  • Jefferies, R. P. S. (1986) The ancestry of the Vertebrates, British Museum (Natural History), London.

    Google Scholar 

  • Jollie, M. T. (1977) Segmentation of the vertebrate head. Am. Zool. 17: 323–333.

    Google Scholar 

  • Källen, B. (1956) Experiments on neuromery in Ambystoma punctatum embryos. J. Embryol. Exp. Morphol. 4: 66–72.

    Google Scholar 

  • Kessel, M. (1992) Respecification of vertebral identities by retinoic acid. Development 115: 487–501.

    PubMed  CAS  Google Scholar 

  • Keynes, R. J., Stern, C. D. (1984) Segmentation in the vertebrate nervous system. Nature 310: 786–789.

    Article  PubMed  CAS  Google Scholar 

  • Killian, C. (1891) Zur Metamerie des Selachierkopfes. Verh. anat. Ges. 5: 85–107.

    Google Scholar 

  • Koltzoff, N. K. (1899) Metamerie des Kopfes von Petromyzon planeri. Anat. Anz.

  • Kuratani, S. C. (1991) Alternate expression of the HNK-1 epitope in rhombomeres of the chick embryo. Dev. Biol. 144: 215–219.

    Article  PubMed  CAS  Google Scholar 

  • Kuratani, S. (1997) Distribution of postotic crest cells in the chick embryo defines the trunk/head interface: embryological interpretation of crest cell distribution and evolution of the vertebrate head. Anat. Embryol. 195: 1–13.

    Article  PubMed  CAS  Google Scholar 

  • Kuratani, S., Aizawa, S. (1995) Patterning of the cranial nerve in the chick embryo is dependent on cranial mesoderm and rhombomeric metamerism. Dev. Growth Differ. 37: 717–731.

    Article  Google Scholar 

  • Kuratani, S. C., Bockman, D. E. (1992) Inhibition of epibranchial placode-derived ganglia in the developing rat by bisdiamine. Anat. Rec. 233: 617–624.

    Article  PubMed  CAS  Google Scholar 

  • Kuratani, S. C., Eichele, G. (1993) Rhombomere transplantation repatterns the segmental organization of cranial nerves and reveals cell-autonomous expression of a homeodomain protein. Development 117: 105–117.

    PubMed  CAS  Google Scholar 

  • Kuratani, S., Horigome, N. (2000) Development of peripheral nerves in a cat shark, Scyliorhinus torazame, with special reference to rhombomeres, cephalic mesoderm, and distribution patterns of crest cells. Zool. Sci. 17: 893–909.

    Article  Google Scholar 

  • Kuratani, S., Horigome, N., Hirano, S. (1999) Developmental morphology of the cephalic mesoderm and re-evaluation of segmental theories of the vertebrate head: evidence from embryos of an agnathan vertebrate, Lampetra japonica. Dev. Biol. 210: 381–400.

    Article  PubMed  CAS  Google Scholar 

  • Kuratani, S., Nobusada, Y., Saito, H., Shigetani, Y. (2000) Morphological development of the cranial nerves and mesodermal head cavities in sturgeon embryos from early pharyngula to mid-larval stages. Zool. Sci. 17: 911–933.

    Article  Google Scholar 

  • Lacalli, T. C., Holland, N. D., West, J. E. (1994) Landmarks in the anterior central nervous system of amphioxus larvae. Phil. Trans. R. Soc. Lond. B 344: 165–185.

    Article  Google Scholar 

  • Ladher, R. K., Anakwe, K. U., Gurney, A. L., Schoenwolf, G. C., Francis-West, P. H. (2000) Identification of synergistic signals initiating inner ear development. Science 290: 1965–1967.

    Article  PubMed  CAS  Google Scholar 

  • Le Douarin, N. M. (1982) The Neural Crest, Cambridge University Press, Cambridge.

    Google Scholar 

  • Lehmann, F. (1927) Further studies on the morphogenetic role of somites in the development of the nervous system of amphibians. J. Exp. Zool. 49: 93–131.

    Article  Google Scholar 

  • Lim, T. M., Lunn, E. R., Keynes, R. J., Stern, C. D. (1987) The differing effects of occipital and trunk somites on neural development in the chick embryo. Development 100: 525–533.

    PubMed  CAS  Google Scholar 

  • Lim, T. M., Jaques, K. F., Stern, C. D., Keynes, R. J. (1991) An evaluation of myelomeres and segmentation of the chick embryo spinal cord. Development 113: 227–238.

    PubMed  CAS  Google Scholar 

  • Locy, W. A. (1895) Contributions to the structure and development of the vertebrate head. J. Morphol. 11: 497–594.

    Article  Google Scholar 

  • Lumsden, A., Sprawson, N., Graham, A. (1991) Segmental origin and migration of neural crest cells in the hindbrain region of the chick embryo. Development 113: 1281–1291.

    PubMed  CAS  Google Scholar 

  • Marshall, A. M. (1878) The development of the cranial nerves of the chick. Quart. J. microsc. Sci. 18: 10–40.

    Google Scholar 

  • Marshall, A. M. (1881) On the head cavities and associated nerves in elasmobranchs. Quart. J. microsc. Sci. 21: 72–97.

    Google Scholar 

  • McGinnis, W., Krumlauf, R. (1992) Homeobox genes and axial patterning. Cell 68: 283–302.

    Article  PubMed  CAS  Google Scholar 

  • Meier, S. (1981) Development of the chick embryo mesoblast: morphogenesis of the prechordal plate and cranial segments. Dev. Biol. 83: 49–61.

    Article  PubMed  CAS  Google Scholar 

  • Meier, S., Packard, D. S. Jr. (1984) Morphogenesis of the cranial segments and distribution of neural crest in embryos of the snapping turtle, Chelydra serpentina. Dev. Biol. 102: 309–323.

    Article  PubMed  CAS  Google Scholar 

  • Meier, S., Tam, P. P. L. (1982) Metatmeric pattern development in the embryonic axis of the mouse. I. Differentiation of the cranial segments. Differentiation 21: 95–108.

    Article  PubMed  CAS  Google Scholar 

  • Moody, S. A., Heaton, M. B. (1983a) Developmental relationships between trigeminal ganglia and trigeminal motoneurons in chick embryos. I. Ganglion development is necessary for motoneuron migration. J. Comp. Neurol. 213: 327–343.

    Article  PubMed  CAS  Google Scholar 

  • Moody, S. A., Heaton, M. B. (1983b) Developmental relationships between trigeminal ganglia and trigeminal motoneurons in chick embryos. II. Ganglion axon ingrowth guides motoneuron migration. J. Comp. Neurol. 213: 344–349.

    Article  PubMed  CAS  Google Scholar 

  • Moody, S. A., Heaton, M. B. (1983c) Developmental relationships between trigeminal ganglia and trigeminal motoneurons in chick embryos. III. Ganglion perikarya direct motor axon growth in the periphery. J. Comp. Neurol. 213: 350–364.

    Article  PubMed  CAS  Google Scholar 

  • Murakami, Y., Ogasawara, M., Sugahara, F., Hirano, S., Satoh, N., Kuratani, S. (2001) Identification and expression of the lamprey Pax-6 gene: Evolutionary origin of segmented brain of vertebrates. Development 128: 3521–3531.

    PubMed  CAS  Google Scholar 

  • Neal, H. V. (1898) The segmentation of the nervous system in Squalus acanthias. Bull. Mus. Comp. Zool. 31: 147–294.

    Google Scholar 

  • Neal, H. V. (1918) Neuromeres and metameres. J. Morphol. 31: 293–315.

    Article  Google Scholar 

  • Neal, H. V., Rand, H. W. (1942) Comparative Anatomy, The Blakiston Co., Philadelphia.

    Google Scholar 

  • Niederländer, C., Lumsden, A. (1996) Late emigrating neural crest cells migrate specifically to the exit points of cranial branchiomotor nerves. Development 122: 2367–2374.

    PubMed  Google Scholar 

  • Nieto, M. A., Gilardi-Hebenstreit, P., Charnay, P., Wilkinson, D. G. (1992) A receptor protein tyrosine kinase implicated in the segmental patterning of the hindbrain and mesoderm. Development 116: 1137–1150.

    PubMed  CAS  Google Scholar 

  • Noden, D. M. (1983) The embryonic origins of avian cephalic and cervical muscles and associated connective tissues. Am. J. Anat. 168: 257–276.

    Article  PubMed  CAS  Google Scholar 

  • Noden, D. M. (1988) Interactions and fates of avian craniofacial mesenchyme. Development 103 (Suppl): 121–140.

    PubMed  Google Scholar 

  • Nyhart, L. K. (1995) Biology Takes Form: Animal Morphology and the German Universities, 1800–1900. Univ. Chicago Press, Chicago, London.

    Google Scholar 

  • Oakley, R. A., Lasky, C. J., Erickson, C. A., Tosney, K. W. (1994) Glycoconjugates mark a transient barrier to neural crest migration in the chick embryo. Development 120: 103–114.

    PubMed  CAS  Google Scholar 

  • Oppel, A. (1890) Ueber Vorderkopf Somite und die Kopfhöhle bei Anguis fragilis. Arch. mik. Anat. 36: 603–627.

    Article  Google Scholar 

  • Owen, R. (1848) On the Archetype and Homology of the Vertebrate Skeleton, Voorst, London.

    Google Scholar 

  • Palmeirim, I., Henrique, D., Ish-Horowicz, D., Pourquie, O. (1997) Avian hairy gene expression identifies a molecular clock linked to vertebrate segmentation and somitogenesis. Cell 91: 639–648.

    Article  PubMed  CAS  Google Scholar 

  • Pasqualetti, M., Ori, M., Nardi, I., Rijli, F. M. (2000) Ectopic Hoxa2 induction after neural crest migration results in homeosis of jaw elements in Xenopus. Development 127: 5367–5378.

    PubMed  CAS  Google Scholar 

  • Platt, J. B. (1891) A contribution to the morphology of the vertebrate head, based on a study of Acanthias vulgaris. J. Morphol. 5: 79–106.

    Article  Google Scholar 

  • Platt, J. B. (1894) Ontogenetische Differenzierung des Ectoderms in Necturus. Studie I. Arch. mikr. Anat. 43: 911–966.

    Google Scholar 

  • Rabl, C. (1892) Über die Metamerie des Wirbelthierkopfes. Verh. anat. Ges. 6: 104–135.

    Google Scholar 

  • Raff, R. A. (1996) The Shape of Life, Univ. Chicago Press, Chicago.

    Google Scholar 

  • Rickmann, M., Fawcett, J. W., Keynes, R. (1985) Ther migration of neural crest cells and the growth of motor axons through the rostral half of the chick somite. J. Emb. Exp. Morphol. 90: 437–455.

    CAS  Google Scholar 

  • Riedl, R. (1978) Order in Living Organisms, Wiley Press, Chichester, New York.

    Google Scholar 

  • Rijli, F. M., Mark, M., Lakkaraju, S., Dierich, A., Dollé, P., Chambon, P. (1993) Homeotic transformation is generated in the rostral branchial region of the head by disruption of Hoxa-2, which acts as a selector gene. Cell 75: 1333–1349.

    Article  PubMed  CAS  Google Scholar 

  • Romer, A. S. (1972) The vertebrate as a dual animal - somatic and visceral. Evol. Biol. 6: 121–156.

    Google Scholar 

  • Romer, A. S., Parsons, T. S. (1977) The Vertebrate Body 5th Ed., Saunders, Philadelphia.

    Google Scholar 

  • Sander, K. (1983) The evolution of patterning mechanisms: gleanings from insect embryogenesis. In: Goodwin, B. C., Holder, N., Wilie, C. C. (eds) Development and Evolution, Cambridge. Cambridge Univ. Press, pp 137–159.

    Google Scholar 

  • Sechrist, J., Serbedzija, G. N., Sherson T., Fraser, S., Bronner-Fraser, M. (1993) Segmental migration of the hindbrain neural crest does not arise from segmental generation. Development 118: 691–703.

    PubMed  CAS  Google Scholar 

  • Sewertzoff, A. N. (1899) Die Entwicklung des Selachierschaedels. Festschr. f. L. v. Kupffer, Jena, 1899.

    Google Scholar 

  • Shigetani, Y., Aizawa, S., Kuratani, S. (1995) Overlapping origins of pharyngeal arch crest cells on the postotic hindbrain. Dev. Growth Differ. 37: 733–746.

    Article  Google Scholar 

  • Singer, C. (1989) A History of Biology to About the Year 1900: a general introduction to the study of living things. Iowa State Univ. Press, Iowa.

    Google Scholar 

  • Slack, J. M. W., Holland, P. W. H., Graham, C. F. (1993) The zootype and the phylotypic stage. Nature 361: 490–492.

    Article  PubMed  CAS  Google Scholar 

  • Smith, A., Robinson, V., Patel, K., Wilkinson, D. G. (1997) The EphA4 and EphB1 receptor tyrosine kinases and ephrin-B2 ligand regulate targeted migration of branchial neural crest cells. Curr. Biol. 7: 561–570.

    Article  PubMed  CAS  Google Scholar 

  • Starck, D. (1963) Die Metamerie des Kopfes der Wirbeltiere. Zool. Anz. 170: 393–428.

    Google Scholar 

  • Teillet, A. M., Kalcheim, K., LeDouarin, N. M. (1987) Formation of the dorsal root ganglia in the avian embryo: Segmental origin and migratory behavior of neural crest progenitor cells. Dev. Biol. 120: 329–347.

    Article  PubMed  CAS  Google Scholar 

  • Tosney, K. W. (1982) The segregation and early migration of cranial neural crest cells in the avian embryo. Dev. Biol. 89: 13–24.

    Article  PubMed  CAS  Google Scholar 

  • Veitch, E., Begbie, J., Schilling, T. F., Smith, M. M., Graham, A. (1999) Pharyngeal arch patterning in the absence of neural crest. Curr. Biol. 9: 1481–1484.

    Article  PubMed  CAS  Google Scholar 

  • Wachtler, F., Jacob, M. (1986) Origin and development of the cranial skeletal muscles. Biblthka Anat. 29: 24–46.

    Google Scholar 

  • Wachtler, F., Jacob, H. J., Jacob, M., Christ, B. (1984) The extrinsic ocular muscles in birds are derived from the prechordal mesoderm. Naturewiss. 71: 379–380.

    Article  CAS  Google Scholar 

  • Wagner, G. P. (1994) homology and the mechanisms of development. In: B. K. Hall ed. Homology: the hierarchical basis of comparative biology, Academic Press, San Diego. pp 273–299.

    Google Scholar 

  • Wedin, B. (1949) The development of the head cavities in Alligator mississippiensis Daud. Lunds Univ. Arssikr. N. F. avs. 2, 45: 1–32 (cited in Starck 1963).

    Google Scholar 

  • van Wijhe, J. W. (1882). Über die Mesodermsegmente und die Entwicklung der Nerven des Selachierkopfes. Ver. Akad. Wiss. 22: 1–50.

    Google Scholar 

  • Ziegler, H. E. (1908) Die phylogenetische Entstehung des Kopfes der Wirbeltiere. Jena Z. Naturw. 43: 653–684.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Shigeru Kuratani PhD.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kuratani, S. Evolutionary developmental biology and vertebrate head segmentation: A perspective from developmental constraint. Theory Biosci. 122, 230–251 (2003). https://doi.org/10.1007/s12064-003-0055-6

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12064-003-0055-6

Key words

Navigation