Skip to main content
Journal of Anatomy logoLink to Journal of Anatomy
. 2001 Jul-Aug;199(Pt 1-2):105–119. doi: 10.1046/j.1469-7580.2001.19910105.x

Neural crest patterning and the evolution of the jaw

CHARLES B KIMMEL 1 ,, CRAIG T MILLER 1 , ROGER J KEYNES 2
PMCID: PMC1594948  PMID: 11523812

Abstract

Here we present ideas connecting the behaviour of the cranial neural crest during development with the venerable, perhaps incorrect, view that gill-supporting cartilages of an ancient agnathan evolved into the skeleton of an early gnathostome's jaw. We discuss the pattern of migration of the cranial neural crest ectomesenchyme in zebrafish, along with the subsequent arrangement of postmigratory crest and head mesoderm in the nascent pharyngeal segments (branchiomeres), in diverse gnathostomes and in lampreys. These characteristics provide for a plausible von Baerian explanation for the problematic inside-outside change in topology of the gills and their supports between these 2 major groups of vertebrates. We consider it likely that the jaw supports did indeed arise from branchiomeric cartilages.

Keywords: Jaw evolution, neural crest, branchial arches, pharyngeal arches

Full Text

The Full Text of this article is available as a PDF (599.9 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Akimenko M. A., Ekker M., Wegner J., Lin W., Westerfield M. Combinatorial expression of three zebrafish genes related to distal-less: part of a homeobox gene code for the head. J Neurosci. 1994 Jun;14(6):3475–3486. doi: 10.1523/JNEUROSCI.14-06-03475.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Ang S. L., Conlon R. A., Jin O., Rossant J. Positive and negative signals from mesoderm regulate the expression of mouse Otx2 in ectoderm explants. Development. 1994 Oct;120(10):2979–2989. doi: 10.1242/dev.120.10.2979. [DOI] [PubMed] [Google Scholar]
  3. Bulfone A., Kim H. J., Puelles L., Porteus M. H., Grippo J. F., Rubenstein J. L. The mouse Dlx-2 (Tes-1) gene is expressed in spatially restricted domains of the forebrain, face and limbs in midgestation mouse embryos. Mech Dev. 1993 Mar;40(3):129–140. doi: 10.1016/0925-4773(93)90071-5. [DOI] [PubMed] [Google Scholar]
  4. Clouthier D. E., Hosoda K., Richardson J. A., Williams S. C., Yanagisawa H., Kuwaki T., Kumada M., Hammer R. E., Yanagisawa M. Cranial and cardiac neural crest defects in endothelin-A receptor-deficient mice. Development. 1998 Mar;125(5):813–824. doi: 10.1242/dev.125.5.813. [DOI] [PubMed] [Google Scholar]
  5. Clouthier D. E., Williams S. C., Yanagisawa H., Wieduwilt M., Richardson J. A., Yanagisawa M. Signaling pathways crucial for craniofacial development revealed by endothelin-A receptor-deficient mice. Dev Biol. 2000 Jan 1;217(1):10–24. doi: 10.1006/dbio.1999.9527. [DOI] [PubMed] [Google Scholar]
  6. Degenhardt K., Sassoon D. A. A role for Engrailed-2 in determination of skeletal muscle physiologic properties. Dev Biol. 2001 Mar 1;231(1):175–189. doi: 10.1006/dbio.2000.0131. [DOI] [PubMed] [Google Scholar]
  7. Depew M. J., Liu J. K., Long J. E., Presley R., Meneses J. J., Pedersen R. A., Rubenstein J. L. Dlx5 regulates regional development of the branchial arches and sensory capsules. Development. 1999 Sep;126(17):3831–3846. doi: 10.1242/dev.126.17.3831. [DOI] [PubMed] [Google Scholar]
  8. Gans C., Northcutt R. G. Neural crest and the origin of vertebrates: a new head. Science. 1983 Apr 15;220(4594):268–273. doi: 10.1126/science.220.4594.268. [DOI] [PubMed] [Google Scholar]
  9. Graham A, Koentges G, Lumsden A. Neural Crest Apoptosis and the Establishment of Craniofacial Pattern: An Honorable Death. Mol Cell Neurosci. 1996 Aug;8(2/3):76–83. doi: 10.1006/mcne.1996.0046. [DOI] [PubMed] [Google Scholar]
  10. Hacker A., Guthrie S. A distinct developmental programme for the cranial paraxial mesoderm in the chick embryo. Development. 1998 Sep;125(17):3461–3472. doi: 10.1242/dev.125.17.3461. [DOI] [PubMed] [Google Scholar]
  11. Hatta K., Schilling T. F., BreMiller R. A., Kimmel C. B. Specification of jaw muscle identity in zebrafish: correlation with engrailed-homeoprotein expression. Science. 1990 Nov 9;250(4982):802–805. doi: 10.1126/science.1978412. [DOI] [PubMed] [Google Scholar]
  12. Henry C. A., Hall L. A., Burr Hille M., Solnica-Krezel L., Cooper M. S. Somites in zebrafish doubly mutant for knypek and trilobite form without internal mesenchymal cells or compaction. Curr Biol. 2000 Sep 7;10(17):1063–1066. doi: 10.1016/s0960-9822(00)00677-1. [DOI] [PubMed] [Google Scholar]
  13. Horigome N., Myojin M., Ueki T., Hirano S., Aizawa S., Kuratani S. Development of cephalic neural crest cells in embryos of Lampetra japonica, with special reference to the evolution of the jaw. Dev Biol. 1999 Mar 15;207(2):287–308. doi: 10.1006/dbio.1998.9175. [DOI] [PubMed] [Google Scholar]
  14. Keynes R., Lumsden A. Segmentation and the origin of regional diversity in the vertebrate central nervous system. Neuron. 1990 Jan;4(1):1–9. doi: 10.1016/0896-6273(90)90438-l. [DOI] [PubMed] [Google Scholar]
  15. Kimmel C. B., Miller C. T., Moens C. B. Specification and morphogenesis of the zebrafish larval head skeleton. Dev Biol. 2001 May 15;233(2):239–257. doi: 10.1006/dbio.2001.0201. [DOI] [PubMed] [Google Scholar]
  16. Kulesa P. M., Fraser S. E. In ovo time-lapse analysis of chick hindbrain neural crest cell migration shows cell interactions during migration to the branchial arches. Development. 2000 Mar;127(6):1161–1172. doi: 10.1242/dev.127.6.1161. [DOI] [PubMed] [Google Scholar]
  17. Kuratani S., Horigome N., Hirano S. Developmental morphology of the head mesoderm and reevaluation of segmental theories of the vertebrate head: evidence from embryos of an agnathan vertebrate, Lampetra japonica. Dev Biol. 1999 Jun 15;210(2):381–400. doi: 10.1006/dbio.1999.9266. [DOI] [PubMed] [Google Scholar]
  18. Köntges G., Lumsden A. Rhombencephalic neural crest segmentation is preserved throughout craniofacial ontogeny. Development. 1996 Oct;122(10):3229–3242. doi: 10.1242/dev.122.10.3229. [DOI] [PubMed] [Google Scholar]
  19. Lee K. H., Xu Q., Breitbart R. E. A new tinman-related gene, nkx2.7, anticipates the expression of nkx2.5 and nkx2.3 in zebrafish heart and pharyngeal endoderm. Dev Biol. 1996 Dec 15;180(2):722–731. doi: 10.1006/dbio.1996.0341. [DOI] [PubMed] [Google Scholar]
  20. Lumsden A., Krumlauf R. Patterning the vertebrate neuraxis. Science. 1996 Nov 15;274(5290):1109–1115. doi: 10.1126/science.274.5290.1109. [DOI] [PubMed] [Google Scholar]
  21. Maemura K., Kurihara H., Kurihara Y., Oda H., Ishikawa T., Copeland N. G., Gilbert D. J., Jenkins N. A., Yazaki Y. Sequence analysis, chromosomal location, and developmental expression of the mouse preproendothelin-1 gene. Genomics. 1996 Jan 15;31(2):177–184. doi: 10.1006/geno.1996.0029. [DOI] [PubMed] [Google Scholar]
  22. Martindale M. Q., Meier S., Jacobson A. G. Mesodermal metamerism in the teleost, Oryzias latipes (the medaka). J Morphol. 1987 Sep;193(3):241–252. doi: 10.1002/jmor.1051930303. [DOI] [PubMed] [Google Scholar]
  23. Metscher B. D., Ahlberg P. E. Zebrafish in context: uses of a laboratory model in comparative studies. Dev Biol. 1999 Jun 1;210(1):1–14. doi: 10.1006/dbio.1999.9230. [DOI] [PubMed] [Google Scholar]
  24. Miller C. T., Schilling T. F., Lee K., Parker J., Kimmel C. B. sucker encodes a zebrafish Endothelin-1 required for ventral pharyngeal arch development. Development. 2000 Sep;127(17):3815–3828. doi: 10.1242/dev.127.17.3815. [DOI] [PubMed] [Google Scholar]
  25. Miyake T., McEachran J. D., Hall B. K. Edgeworth's legacy of cranial muscle development with an analysis of muscles in the ventral gill arch region of batoid fishes (Chondrichthyes: Batoidea). J Morphol. 1992 Jun;212(3):213–256. doi: 10.1002/jmor.1052120304. [DOI] [PubMed] [Google Scholar]
  26. Moens C. B., Cordes S. P., Giorgianni M. W., Barsh G. S., Kimmel C. B. Equivalence in the genetic control of hindbrain segmentation in fish and mouse. Development. 1998 Feb;125(3):381–391. doi: 10.1242/dev.125.3.381. [DOI] [PubMed] [Google Scholar]
  27. Morrison S. L., Campbell C. K., Wright G. M. Chondrogenesis of the branchial skeleton in embryonic sea lamprey, Petromyzon marinus. Anat Rec. 2000 Nov 1;260(3):252–267. doi: 10.1002/1097-0185(20001101)260:3<252::AID-AR50>3.0.CO;2-4. [DOI] [PubMed] [Google Scholar]
  28. Neidert A. H., Virupannavar V., Hooker G. W., Langeland J. A. Lamprey Dlx genes and early vertebrate evolution. Proc Natl Acad Sci U S A. 2001 Feb 13;98(4):1665–1670. doi: 10.1073/pnas.98.4.1665. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Noden D. M. The embryonic origins of avian cephalic and cervical muscles and associated connective tissues. Am J Anat. 1983 Nov;168(3):257–276. doi: 10.1002/aja.1001680302. [DOI] [PubMed] [Google Scholar]
  30. Ogasawara M., Shigetani Y., Hirano S., Satoh N., Kuratani S. Pax1/Pax9-Related genes in an agnathan vertebrate, Lampetra japonica: expression pattern of LjPax9 implies sequential evolutionary events toward the gnathostome body plan. Dev Biol. 2000 Jul 15;223(2):399–410. doi: 10.1006/dbio.2000.9756. [DOI] [PubMed] [Google Scholar]
  31. Peters H., Neubüser A., Kratochwil K., Balling R. Pax9-deficient mice lack pharyngeal pouch derivatives and teeth and exhibit craniofacial and limb abnormalities. Genes Dev. 1998 Sep 1;12(17):2735–2747. doi: 10.1101/gad.12.17.2735. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Piotrowski T., Nüsslein-Volhard C. The endoderm plays an important role in patterning the segmented pharyngeal region in zebrafish (Danio rerio). Dev Biol. 2000 Sep 15;225(2):339–356. doi: 10.1006/dbio.2000.9842. [DOI] [PubMed] [Google Scholar]
  33. Piotrowski T., Schilling T. F., Brand M., Jiang Y. J., Heisenberg C. P., Beuchle D., Grandel H., van Eeden F. J., Furutani-Seiki M., Granato M. Jaw and branchial arch mutants in zebrafish II: anterior arches and cartilage differentiation. Development. 1996 Dec;123:345–356. doi: 10.1242/dev.123.1.345. [DOI] [PubMed] [Google Scholar]
  34. Pourquié O. Vertebrate segmentation: is cycling the rule? Curr Opin Cell Biol. 2000 Dec;12(6):747–751. doi: 10.1016/s0955-0674(00)00163-0. [DOI] [PubMed] [Google Scholar]
  35. Pöpperl H., Rikhof H., Chang H., Haffter P., Kimmel C. B., Moens C. B. lazarus is a novel pbx gene that globally mediates hox gene function in zebrafish. Mol Cell. 2000 Aug;6(2):255–267. doi: 10.1016/s1097-2765(00)00027-7. [DOI] [PubMed] [Google Scholar]
  36. Robinson G. W., Mahon K. A. Differential and overlapping expression domains of Dlx-2 and Dlx-3 suggest distinct roles for Distal-less homeobox genes in craniofacial development. Mech Dev. 1994 Dec;48(3):199–215. doi: 10.1016/0925-4773(94)90060-4. [DOI] [PubMed] [Google Scholar]
  37. Sadaghiani B., Thiébaud C. H. Neural crest development in the Xenopus laevis embryo, studied by interspecific transplantation and scanning electron microscopy. Dev Biol. 1987 Nov;124(1):91–110. doi: 10.1016/0012-1606(87)90463-5. [DOI] [PubMed] [Google Scholar]
  38. Schilling T. F. Genetic analysis of craniofacial development in the vertebrate embryo. Bioessays. 1997 Jun;19(6):459–468. doi: 10.1002/bies.950190605. [DOI] [PubMed] [Google Scholar]
  39. Schilling T. F., Kimmel C. B. Musculoskeletal patterning in the pharyngeal segments of the zebrafish embryo. Development. 1997 Aug;124(15):2945–2960. doi: 10.1242/dev.124.15.2945. [DOI] [PubMed] [Google Scholar]
  40. Schilling T. F., Kimmel C. B. Segment and cell type lineage restrictions during pharyngeal arch development in the zebrafish embryo. Development. 1994 Mar;120(3):483–494. doi: 10.1242/dev.120.3.483. [DOI] [PubMed] [Google Scholar]
  41. Tam P. P., Trainor P. A. Specification and segmentation of the paraxial mesoderm. Anat Embryol (Berl) 1994 Apr;189(4):275–305. doi: 10.1007/BF00190586. [DOI] [PubMed] [Google Scholar]
  42. Tomsa J. M., Langeland J. A. Otx expression during lamprey embryogenesis provides insights into the evolution of the vertebrate head and jaw. Dev Biol. 1999 Mar 1;207(1):26–37. doi: 10.1006/dbio.1998.9163. [DOI] [PubMed] [Google Scholar]
  43. Trainor P. A., Manzanares M., Krumlauf R. Genetic interactions during hindbrain segmentation in the mouse embryo. Results Probl Cell Differ. 2000;30:51–89. doi: 10.1007/978-3-540-48002-0_3. [DOI] [PubMed] [Google Scholar]
  44. Trainor P. A., Tam P. P. Cranial paraxial mesoderm and neural crest cells of the mouse embryo: co-distribution in the craniofacial mesenchyme but distinct segregation in branchial arches. Development. 1995 Aug;121(8):2569–2582. doi: 10.1242/dev.121.8.2569. [DOI] [PubMed] [Google Scholar]
  45. Trainor P. A., Tan S. S., Tam P. P. Cranial paraxial mesoderm: regionalisation of cell fate and impact on craniofacial development in mouse embryos. Development. 1994 Sep;120(9):2397–2408. doi: 10.1242/dev.120.9.2397. [DOI] [PubMed] [Google Scholar]
  46. Trainor P., Krumlauf R. Plasticity in mouse neural crest cells reveals a new patterning role for cranial mesoderm. Nat Cell Biol. 2000 Feb;2(2):96–102. doi: 10.1038/35000051. [DOI] [PubMed] [Google Scholar]
  47. Ueki T., Kuratani S., Hirano S., Aizawa S. Otx cognates in a lamprey, Lampetra japonica. Dev Genes Evol. 1998 Jun;208(4):223–228. doi: 10.1007/s004270050176. [DOI] [PubMed] [Google Scholar]
  48. Veitch E., Begbie J., Schilling T. F., Smith M. M., Graham A. Pharyngeal arch patterning in the absence of neural crest. Curr Biol. 1999 Dec 16;9(24):1481–1484. doi: 10.1016/s0960-9822(00)80118-9. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Anatomy are provided here courtesy of Anatomical Society of Great Britain and Ireland

RESOURCES