Skip to main content
Log in

The fate map of the chick forelimb-bud and its bearing on hypothesized developmental control mechanisms

  • Original Articles
  • Published:
Anatomy and Embryology Aims and scope Submit manuscript

Summary

Carbon particles and isotopic quail grafts were used as markers to study the salient features of the fate map of the chick forelimb between stages 20 and 27. The grafting technique confirmed the reliability of the carbon method: they both revealed striking asymmetries in which apical mesodermal tissue was progressively displaced in a proximal direction (as would be expected on the basis of growth by net apical addition of tissue) but also in a preaxial direction, while postaxial tissue became elongated in the direction of limb outgrowth. Ectoderm showed a similar preaxial-postaxial asymmetry but became displaced from initially underlying mesoderm. In marked contrast to mesoderm, distal ectoderm remained at a constant distance from the apical ectodermal ridge (or became incorporated into it), thus implying that the ectodermal sheet is anchored distally and grows by uniform stretching proximally. Within the ectoderm itself, the outer peridermal layer is displaced distally relative to the underlying epidermal basal layer. Peripheral mesoderm showed patterns of displacement which were intermediate between those of ectoderm and chondrogenic core mesoderm. It is argued that such morphogenetic phenomena are integral components of developmental mechanisms of significance in the control of pattern generation. Implications of the interpretation and use of the fate map in relation to theories of limb development, particularly those based on mechanisms defined in terms of limb axes, are reviewed.

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

  • Amprino R (1965) Aspects of limb morphogenesis in the chicken. In: DeHaan RL, Ursprung H (eds) Organogenesis, Holt, Rinehart and Winston, New York, pp 255–281

    Google Scholar 

  • Amprino R (1976) On the topography of the presumptive skeletal mesenchyme in the early wing bud of chick embryos. Arch Biol Brux 87:1–41

    Google Scholar 

  • Amprino R (1977) Further observations on the site of bone prospective areas in the chick embryo wing bud. Acta Anat 98:295–312

    Google Scholar 

  • Amprino R (1979) Developmental interactions between the adjacent parts of combined heterologous skeletogenous territories. Anat Embryol 155:135–148

    Google Scholar 

  • Amprino R, Ambrosi G (1973) Experimental analysis of the chick embryo limb bud growth. Arch Biol Brux 84:35–86

    Google Scholar 

  • Amprino R, Camosso ME (1956) Etude expérimentale de la morphogenèse de l'aile dans l'embryon de Poulet. I. Recherches par la methode des marques colorées. Arch Biol Brux 67:613–633

    Google Scholar 

  • Amprino R, Camosso ME (1958) Anilisi sperimentale dello sviluppo dell'ala nell'embrione di pollo. Roux Arch Entw-Mech Organ 150:509–541

    Google Scholar 

  • Bellairs R (1953) Studies on the development of the foregut in the chick blastoderm. I. The presumptive foregut area. J Embryol Exp Morphol 1:115–124

    Google Scholar 

  • Blechschmidt E (1956) Entwicklungsfunktionelle Untersuchungen am Bewegungsapparat. Acta Anat 27:62–88

    Google Scholar 

  • Brand B, Christ B, Jacob HJ (1985) An experimental analysis of the developmental capacities of distal parts of avian leg buds. Am J Anatomy 173:321–340

    Google Scholar 

  • Cairns JM (1977) Growth of normal and talpid 2 chick wing buds: an experimental analysis. In: Ede DA, Hinchliffe JR, Balls M (eds) Vertebrate limb and somite morphogenesis. Third Symposium of the British Society for Developmental Biology, Cambridge University Press, Cambridge, pp 123–137

    Google Scholar 

  • Camosso ME, Roncali L (1968) Time sequence of the processes of ectodermal ridge thickening and of mesodermal cell proliferation during apical outgrowth of the chick embryo wing bud. Acta Embryol Morphol Exp 10:247–263

    Google Scholar 

  • Camosso M, Jacobelli V, Pappalettera N (1957) Studio sulla morfologenesi dell'ala nell'embrione di pollo. (I) Distribuzione delle mitosi nell'ectoderma. Boll Soc Ital Biol Sper 33:595–598

    Google Scholar 

  • Chaube S (1959) On axiation and symmetry in transplanted wing of the chick. J Exp Zool 140:29–77

    Google Scholar 

  • Cooke J, Summerbell D (1980) Cell cycle and experimental pattern duplication in the chick wing during embryonic development. Nature 287:697–701

    Google Scholar 

  • Cottrill CP (1983) Fate maps and the chick limb bud: a new method. J Anat 136:617–618P

    Google Scholar 

  • Doskocil M (1978) Increase in volume of the chick wing bud at the beginning of its development. Med Biol 56:310–316

    Google Scholar 

  • Ede DA, Flint OP, Teague P (1975) Cell proliferation in the developing wing-bud of normal and talpid 3 mutant chick embryos. J Embryol Exp Morphol 34:589–607

    Google Scholar 

  • Feinberg RN, Repo MA, Saunders JW (1983) Ectodermal control of the avascular zone of the peripheral mesoderm in the chick embryo. J Exp Zool 226:391–398

    Google Scholar 

  • Fell HB, Canti RG (1935) Experiments on the development in vitroof the avian knee-joint. Proc R Soc B 116:316–351

    Google Scholar 

  • Gumpel-Pinot M, Ede DA, Flint OP, (1984) Myogenic cell movement in the developing avian limb bud in presence and absence of the apical ectodermal ridge (AER). J Embryol Exp Morphol 80:105–125

    Google Scholar 

  • Hamburger V, Hamilton HL (1951) A series of normal stages in the development of the chick embryo J Morphol 88:49–92

    Google Scholar 

  • Hampé A (1959) Contributions a l'étude du développement et de la régulation des deficiences et des excédents dans la patte de l'embryon de Poulet. Arch Anat Microsc Morphol Exp 48:345–478

    Google Scholar 

  • Hinchliffe JR, Gumpel-Pinot M (1981) Control of maintenance and antero-posterior skeletal differentiation of the anterior mesenchyme of the chick wing bud by its posterior margin (the ZPA). J Embryol Exp Morphol 62:63–82

    Google Scholar 

  • Hinchliffe JR, Gumpel-Pinot M, Wilson DJ, Yallup BL (1984) The prospective skeletal areas of the chick wing-bud: their location and time of determination in the limb field. Prog Clin Biol Res 151:453–470

    Google Scholar 

  • Horder TJ (1978) Functional adaptibility and morphogenetic opportunism, the only rules for limb development? Zoon 6:181–192

    Google Scholar 

  • Hornbruch A, Wolpert L (1970) Cell division in the early growth and morphogenesis of the chick limb. Nature 226:764–766

    Google Scholar 

  • Javois LC (1984) Pattern specification in the developing chick limb. In: Malacinski GM (ed) Pattern formation. Macmillan, New York, pp 557–579

    Google Scholar 

  • Lavois LC, Iten LE (1982) Supernumerary limb structures after juxtaposing dorsal and ventral chick wing bud cells. Dev Biol 90:127–143

    Google Scholar 

  • Kieny M (1975) Effets de la vinblastine sur la morphogenèse du pied de l'embryon de poulet. Aspects histologíques. J Embryol Exp Morphol 34:609–632

    Google Scholar 

  • Kieny M, Pautou MP (1976) Régulation des excédents dans le développement du bourgeon de membre de l'embryon d'oiseau. Analyse expérimentale de combinaisons xenoplastiques caille/poulet. Roux Arch Ent-Mech Organ 179:327–338

    Google Scholar 

  • Kieny M, Pautou MP, Chevallier A, Mauger A (1986) Spatial organization of the developing limb musculature in birds and mammals. Bibl Anat 29:65–90

    Google Scholar 

  • Le Douarin NM (1969) Particularités du noyau interphasique chez la Caille japonaise (Coturnix coturnix Japonica). Utilisation de ces particularités comme “marquage biologique” dans les recherches sur les interactions tissulaires et les migrations cellulaires au cours de l'ontogenèse. Bull Biol Fr Belg 103:435–452

    Google Scholar 

  • Lewis JH (1977) Growth and determination in the developing limb. In: Ede DA, Hinchliffe JR, Balls M (eds.) Vertebrate limb and somite morphogenesis. Third Symposium of the British Society for Developmental Biology, Cambridge University Press, Cambridge, pp 215–228

    Google Scholar 

  • Lipton BH, Jacobson AG (1974) Analysis of normal somite development. Dev Biol 38:73–90

    Google Scholar 

  • MacCabe JA, Errick J, Saunders JW (1974) Ectodermal control of the dorso ventral axis in the leg bud of the chick embryo. Dev Biol 39:69–82

    Google Scholar 

  • Milaire J (1962) Histochemical aspects of limb morphogenesis in vertebrates. Adv Morphol 2:183–209

    Google Scholar 

  • Milaire J (1973) Indices d'une participation morphogène de l'épiblaste au cours du développement des membres chez les Mammifères. Arch Biol 84:87–114

    Google Scholar 

  • Milaire J (1977) Histochemical expression of morphogenestic gradients during limb morphogenesis (with particular reference to mammalian embryos). Birth Defects 13:37–67

    Google Scholar 

  • Murray PDF, Huxley JS (1925) Self-differentiation in the grafted limb-bud of the chick. J Anat 59:379–384

    Google Scholar 

  • Saunders JW (1948) The proximo-distal sequence of origin of the parts of the chick wing and the role of the ectoderm. J Exp Zool 108:363–402

    Google Scholar 

  • Saunders JW (1958) Inductive specificity in the origin of integumentary derivatives in the fowl. In: McElroy WD, Glass B (eds) The chemical basis of development. John Hopkins Press, Baltimore, pp 239–253

    Google Scholar 

  • Saunders JW, Gasseling MT (1983) New insights into the problem of pattern regulation in the limb bud of the chick embryo. In: Fallon JF, Caplan AI (eds) Limb development and regeneration Part A. Alan R Liss, New York, pp 67–76

    Google Scholar 

  • Saunders JW, Gasseling MT, Saunders LC (1962) Cellular death in morphogenesis of the avian wing. Dev Biol 5:147–178

    Google Scholar 

  • Saunders JW, Gasseling MT, Errick JE (1976) Inductive activity and enduring cellular constitution of a supernumerary apical ectodermal ridge grafted to the limb bud of the chick embryo. Dev Biol 50:16–25

    Google Scholar 

  • Seichert V (1966) Differential growth pattern in the chick embryo wing-bud between the 3.5th and 7th day of incubation. Folia Morphol (Praha) 14:325–333

    Google Scholar 

  • Seichert V (1966) Growth changes in the limb bud of the chick wing in the period of morphogenetic differentiation of the zeugopodium. Folia Morphol (Praha) 16:304–311

    Google Scholar 

  • Seichert V (1979) The spatial interrelationship of the body wall mesoderm and ectoderm of the chick embryo at the level of the developing limbs. Folia Morphol (Praha) 27:310–317

    Google Scholar 

  • Solursh M, Meier S (1986) The distribution of somite-derived myogenic cells during early development of the wing bud. In: Bellairs R, Ede DA, Lash JW (eds) Somites in Developing Embryos. NATO ASI Series A, vol 118. Plenum, New York, pp 277–287

    Google Scholar 

  • Spratt NT (1955) Analysis of the organizer center in the early chick embryo. 1. Localization of prospective notochord and somite cells. J Exp Zool 128:121–163

    Google Scholar 

  • Stark RJ, Searls RL (1973) A description of chick wing bud development and a model of limb morphogenesis. Dev Biol 33:138–153

    Google Scholar 

  • Stopak D, Harris AK (1982) Connective tissue morphogenesis by fibroblast traction. 1. Tissue culture observations. Dev Biol 90:383–398

    Google Scholar 

  • Summerbell D (1977) Reduction of the rate of outgrowth, cell density, and cell division following removal of the apical ectodermal ridge of the chick limb-bud J Embryol Exp Morphol 40:1–21

    Google Scholar 

  • Summerbell D (1979) The zone of polarizing activity: evidence for a role in normal chick limb morphogenesis. J Embryol Exp Morphol 50:217–233

    Google Scholar 

  • Summerbell D, Honig LS (1982) The control of pattern across the antero-posterior axis of the chick limb bud by a unique signalling region. Am Zool 22:105–116

    Google Scholar 

  • Summerbell D, Wolpert L (1972) Cell density and cell division in the early morphogenesis of the chick wing. Nature, New Biology 239:24–26

    Google Scholar 

  • Tickle C (1980) The polarizing region and limb development. In: Johnson MH (ed) Development in Mammals, vol 4. Elsevier, Amsterdam, pp 101–136

    Google Scholar 

  • Tschumi PA (1957) The growth of the hindlimb bud of Xenopus laevis and its dependence upon the epidermis. J Anat 91:149–173

    Google Scholar 

  • Wachtler F (1984) On the differentiation and migration of some non-neuronal neural crest derived cell types. Anat Embryol 170:161–168

    Google Scholar 

  • Waddington CH (1950) Processes of induction in the early development of the chick. L'Année Biol 26:711–717

    Google Scholar 

  • Wilson D (1983) The origin of the endothelium in the developing marginal vein of the chick wing-bud. Cell Differentiation 13:63–67

    Google Scholar 

  • Wolpert L, Lewis J, Summerbell D (1975) Morphogenesis of the vertebrate limb. In: Porter R, Rivers J (eds) Cell patterning, Ciba Foundation Symposium, No 29, (new series), Associated Scientific Publ, Amsterdam, pp 95–119

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bowen, J., Hinchliffe, J.R., Horder, T.J. et al. The fate map of the chick forelimb-bud and its bearing on hypothesized developmental control mechanisms. Anat Embryol 179, 269–283 (1989). https://doi.org/10.1007/BF00326592

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00326592

Key words

Navigation