Abstract
Although several theoretical approaches consider general methods for dealing with shape, recent observations and experimental data show that embryos exhibit marked changes in the properties of the biological material involved in shape development and shape regulation capacity. In vivo experiments have shown that the amphibian embryo gradually develops from a situation in which it is not able to maintain its shape to one in which it can not only maintain its shape but also possesses a maximal tolerance towards deformation together with a maximal shape regulation capacity. So far two especially clear conclusions have emerged: (i) the form of the embryo appears to be determined by cell activities intrinsic to each stage, and (ii) the morphogenetic programme can be executed normally within wide limits notwithstanding dramatic deformations of the embryo during quite a long period. Thus the hypothesis may be advanced that shape and morphogenesis to some extent become independent phenomena during embryonic development.
Similar content being viewed by others
References
Ancel, P. & P. Vintemberger (1948). Recherches sur le déterminisme de la symétrie bilatérale dans l'œuf des amphibiens. - Biol. Bull. 31, p. 1–182.
Babloyantz, A. & J. Hiernaux (1974). Models for positional information and positional differentiation. - Proc. nat. Acad. Sci., USA 71, p. 1530–1533.
Baker, P. C. (1965). Fine structure and morphogenetic movements in the gastrula of the tree frog, Hyla regilla. - J. Cell Biol. 24, p. 95–116.
Baker, P. C. & T. E. Schroeder (1967). Cytoplasmic filaments and morphogenetic movement in the amphibian neural tube. - Developm. Biol. 15, p. 432–450.
Banerjee, S. D., R. H. Cohn & M. R. Bernfield (1977). Basal lamina of embryonic salivary epithelia. Production by the epithelium and role in maintaining lobular morphology. - J. Cell Biol. 73, p. 445–463.
Beloussov, L. V. & J. G. Dorfman (1974). On the mechanics of growth and morphogenesis in hydroid polyps. - Amer. Zool. 14, p. 719–734.
Beloussov, L. V., J. G. Dorfman & V. G. Cherdantzev (1975). Mechanical stresses and morphological patterns in amphibian embryos. - J. Embryol. exp. Morph. 34, p. 559–574.
Bernfield, M. R., S. D. Banerjee & R. H. Cohn (1972). Dependence of salivary epithelial morphology and branching morphogenesis upon acid mucopolysaccharide-protein (proteoglycan) at the epithelial surface. - J. Cell Biol. 52, p. 674–689.
Bernfield, M. R., R. H. Cohn & S. D. Banerjee (1973). Glycosaminoglycans and epithelial organ formation. - Amer. Zool. 13, p. 1067–1083.
Bhisey, A. N. & J. J. Freed (1975). Possible role of microtubules and microfilaments in cell locomotion. - In: G. P. Talwar, ed., Regulation of growth and differentiation in eukaryote cells, p. 155–168. - New York, Raven Press.
Browne, D. A. (1967). Mechanistic interpretation of certain malformation. - In: D. H. M. Woollam, ed., Advances in teratology, vol. 2, p. 11–36. - New York, Logos Press.
Burnside, B. (1971). Microtubules and microfilaments in newt neurulation. - Developm. Biol. 26, p. 416–441.
Bustuoabad, O. & A. Pisanó (1973). Two different patterns of segmentation in the eggs of Bufo arenarum. -Acta Embryol. Exp. 1, p. 29–46.
Byers, B. & K. R. Porter (1974). Oriented microtubules in elongating cells of the developing lens rudiment after induction. - Proc. nat. Acad. Sci., U.S.A. 52, p. 1091–1099.
Bytinski-Salz, H. (1938). Chromatophorenstudien. II. Struktur und Determination des adepidermalen Melanophorennetzes bei Bombina. - Arch. exp. Zellforflh. 22, p. 132–170.
Clavert, J. (1962). Symmetrization of the egg of vertebrates. - Adv. Morphogen. 2, p. 27–60.
Crick, F. (1970). Diffusion in embryogenesis. - Nature, Lond. 225, p. 420–422.
Curtis, A. S. G. & G. van de Vyver (1971). The control of cell adhesion in a morphogenetic system. - J. Embryol. exp. Morph. 26, p. 295–312.
Del Conte, E. & J. Sirlin (1952). Pattern series of the first embryonary stages in Bufo arenarum, Anat. Rec. 112, p. 125–136.
Dunn, P. M. (1976). Congenital postural deformities. - Brit. mod. Bull. 32, p. 71–76.
Ebert, J. D. & I. M. Sussex (1970). Interacting systems in development. 2nd ed. - New York, Holt, Rinehart & Winston, x + 338 pp.
Edelman, G. M. (1976). Surface modulation in cell recognition and cell growth. - Science 192, p. 218–226.
Elsdale, T. & J. Bard (1974). Cellular interactions in morphogenesis of epithelial mesenchymal systems. - Biology 63, p. 343–349.
Faber, J. (1976). Positional information in the amphibian limb. - Acta biotheor., Leiden 25, p. 44–65.
Fawcett, D. M. & F. Witebsky (1964). Observations on the ultrastructure of nucleated erythrocytes and thrombocytes with particular reference to their difloidal shape. - Z. Zellforflh. mikr. Anat. 61, p. 785.
French, V., G. Bryant & S. V. Bryant (1976). Pattern regulation in epimorphic fields. - Science 193, p. 969–981.
Gibbins, J. R., L. G. Tilney & K. R. Porter (1969). Microtubules in the formation and development of the primary mesenchyme in Arbacia punctulata. I. The distribution of microtubules. - J. Cell Biol. 41, p. 201–226.
Goodwin, B. C. & M. H. Cohen (1969). A phase shift model for the spatial and temporal organization in developing systems.-J. theor. Biol. 25, p. 49–107.
Grobstein, C. & J. Cohen (1965). Collagenase: effect on the morphogenesis of embryonic salivary epithelium in vitro. - Science 150, p. 626–628.
Grobstein, C. (1967). Mechanism of organogenetic tissue interactions. - Nat. Cancer Inst. Monogr. 26, p. 279–299.
Gustavson, T. & M. I. Tonebey (1971). How genes control morphogenesis. - Amer. Scient. 59, p. 452–462.
Gustavson, T. & L. Wolpert (1967). Cellular movement and contact in sea urchin morphogenesis. - Biol. Rev. 42, p. 442–498.
Herkovits, J. (1975). Acción de Bromuro de Etidio y del D-Tubocurare en embriones de Bufo arenarum normales y experimentalmente deformados. - Medicina, B. Aires 35, p. 565–566 (abstract).
Herkovits, J. (1976a). Microflopia electrónica de membranas pre-existentes y neoformadas durante un proceso de división celular: la segmentación. - Medicina, B. Aires 36, p. 551 (abstract).
Herkovits, J. (1976b). Limite de viabilidad de embriones que desorrollan con deformaciones experimentales extremas: Las alteraciones del tejido ectodermico. - Medicina, B. Aires 36, p. 551 (abstract).
Herkovits, J. (1977a). Shape regulation capacity during development: Recovery of embryos developing notwithstanding asymmetry until the neurula stage. - Acta Embryol. Exp. 1, p. 3–10.
Herkovits, J. (1977b). Control de la morfogenesis durante el desarrollo embrionario de un affibio: I. Deformaciones experimentales hasta neurula. - Rev. del Inst. de Cibernética de la Soc. Cient. Arg. 1, p. 5–15.
Herkovits, J. (1977c). Are shape and morphogenesis independent phenomena? - Experientia 33, p. 510–513.
Herkovits, J. (1977d). Shape regulation capacity during development: Recovering capacity of embryos developing notwithstanding dramatic deformation. - Acta morph. neerl. fland. 16, p. 69–75.
Herkovits, J. (1977e). Capacidad de recuperación de embriones deformados experimentalmente: etapas de la organogenesis. - Medicina, B. Aires 38, p. 60–68.
Herkovits, J., A. Pisanó & A. F. de Herkovits (1975). Alteraciones en el desarrollo embrionario y en procesos de recuperación morfológica por acción del agua pesada. - Rev. Biol. Med. Nucl. 7, p. 161–162. (abstract).
Herkovits, J., O. Bustuoabad & A. Pisanó (1977). The spatial and temporal pattern of cell activities in the blastocoel cavity of amphibian embryos during archenteron floor descent. - Acta Embryol. Exp. 2, p. 195–205.
Holtfreter, J. (1944). A study of the mechanics of gastrulation: part 2. - J. exp. Zool. 95, p. 171–212.
Karfunkel, P. (1971). The role of microtubules and microfilaments in neurulation in Xenopus. - Developm. Biol. 25, p. 30–56.
Kemp, N. E. (1959). Development of the basement lamella of larval anuran skin. - Developm. Biol. 1, p. 459–476.
Klug, A. & D. L. Caspar (1960). The structure of small viruses. - Adv. Virus Res. 7, p. 225–246.
Lash, J. (1974). Tissue interactions and related subjects. - In: J. Lash & J. R. Whittaker, ed., Concepts of development, p. 197–212. - Stamford, Conn., Sinauer Ass.
Lawrence, B. A. (1971). Control mechanisms of growth and differentiation. - Symp. Soc. exp. Biol. 25, p. 379–390.
Luck, H. B. (1975). Elementary behavioral rules as a foundation for morphogenesis. - J. theor. Biol. 54, p. 23–34.
Martinez, H. M. (1972). Morphogenesis and chemical dissipative structures. A computer simulated case study. - J. theor. Biol. 36, p. 479–501.
Martinov, L. A. (1975). A morphogenetic mechanism involving instability of initial form. - J. theor. Biol. 52, p. 471–480.
Mather, K. (1953). Genetical control of stability in development. - Heredity 7, p. 297–336.
Moflona, A. A. (1965). Recombination of dissociated cells and the development of cell aggregates. - In: E. N. Willmer, ed., Cells and tissues in culture, vol. I, p. 489–529. - New York, Acad. Press.
Moflona, A. A. (1968). Cell aggregation properties of specific cell ligands and their role in the formation of multicellular systems. - Developm. Biol. 18, p. 250–277.
Nakatsuji, N. (1975). Studies on the gastrulation in amphibian embryos: light and electron microscopic observation of a urodele Cynopus pyrrhogaster. - J. Embryol. exp. Morph. 34, p. 669–685.
Overton, J. (1976). Scanning microscopy of collagen in the basement lamella of normal and regenerating frog tadpoles. - J. Morph. 150, p. 805–824.
Perry, M. M. (1975). Microfilaments in the external surface layer of the early amphibian embryo. - J. Embryol. exp. Morph. 33, p. 127–146.
Perry, M. M. & C. H. Waddington (1966). Ultrastructure of the blastopore cells in the newt. - J. Embryol. exp. Morph. 15, p. 317–330.
Porter, K. R. (1966). Cytoplasmic microtubules and their function. - In: G. E. W. Wolstenholme & M. O'Conner, ed., Principles of biomolecular organization. - London, Churchill, 308 pp.
Reeve, E. C. R. & F. W. Robertson (1952). Studies in quantitative inheritance. II. Analysis of a strain of Drosophila melanogaster selected for long wings. - J. Genet. 51, p. 276–316.
Roth, S., E. J. McGuire & S. Rosman (1971). Evidence for cell surface glycosyltransferases: their potential role in cellular recognition. - J. Cell Biol. 51, p. 536–547.
Rutishauser, V., J. P. Thiery, R. Brackenbury, Sela Ben-ami & G. M. Edelman (1976). Mechanism of adhesion among cells from neural tissues of the chick embryo. - Proc. nat. Acad. Sci., U.S.A. 73, p. 577–581.
Schulman, L. S. (1976). Stable generation of simple forms. - J. theor. Biol. 57, p. 453–468.
Shur, B. D. (1977). Cell-surface glycosyltransferases in gastrulating chick embryos. I. Temporally and spatially specific patterns of four endogenous glycosyl-transferase activities. - Developm. Biol. 58, p. 23–39.
Spooner, B. S. (1974). Morphogenesis of vertebrate organs. - In: J. Lash & J. R. Whittaker, ed., Concepts of development, p. 213–241. - Stamford, Conn., Sinauer Ass.
Spooner, B. S. & N. K. Wessells (1972). An analysis of salivary gland morphogenesis: role of cytoplasmic microfilaments and microtubules. - Developm. Biol. 27, p. 38–54.
Steinberg, M. S. (1964). The problem of adhesive selectivity in cellular interactions. - In: M. Locke, ed., Cellular membranes in development, p. 321–366. - New York, Acad. Press.
Steinberg, M. S. (1970). Does differential adhesion govern self-assembly processes in histogenesis? Equilibrium configurations among populations of embryonic cells. - J. exp. Zool. 173, p. 395–434.
Steinberg, M. S. (1975). Adhesion-guided multicellular assembly: a commentary upon the postulates, real and imagined, of the differential adhesion hypothesis, with special attention to computer simulations of cell sorting. - J. theor. Biol. 55, p. 431–443.
Stumpf, H. (1967). About the model of a concentration gradient in the insect segment. - Naturwissenflhaften 54, p. 50–51.
Summerbell, D. & L. Wolpert (1973). Precision of development in chick limb morphogenesis. - Nature, Lond. 224, p. 228–230.
Thom, R. (1972). Stabilité structurelle et morphogenèse. Essai d'une théorie generale des modèles. - Reading, Mass., W. A. Benjamin, 362 pp.
Tilney, L. G. & J. R. Gibbins (1969). Microtubules in the formation and development of the primary mesenchyme in Arbacia punctulata. An experimental analysis of their role in development and maintenance of cell shape. - J. Cell Biol. 41, p. 227–250.
Townes, P. L. & J. Holtfreter (1955). Directed movements and relative adhesion of embryonic amphibian cells. - J. exp. Zool. 128, p. 53–118.
Turing, A. M. (1952). The chemical basis of morphogenesis. - Phil. Trans. R. Soc. B237, p. 37–72.
Ubbels, G. A., R. T. M. Hengst & J. Klag (1975). Cytoplasmic segregation during the symmetrisation of the anuran egg. - Acta morph. neerl. fland. 13, p. 3–4 (abstract).
Weiss, P. (1957). Macromolecular fabrics and pattern. - J. cell. comp. Physiol. 49, p. 105–112.
Weiss, P. (1968). Cell contact. - In: Dynamics of development: Experiments and inferences. Selected papers on developmental biology, p. 343–372. - New York, Acad. Press.
Wessells, N. K. (1970). Mammalian lung development: interactions in formation and morphogenesis of tracheal buds. - J. exp. Zool. 175, p. 455–466.
Wessells, N. K., B. S. Spooner, J. F. Ash, M. O. Bradley, M. A. Ludueňa, E. L. Taylor, J. T. Wrenn & K. M. Yamada (1971). Microfilaments in cellular and developmental processes. - Science 171, p. 135–143.
Wilson, H. V. (1907). On some phenomena of coaleflence and regeneration in sponges. - J. exp. Zool. 5, p. 245–258.
Wolf, K. L. & D. Kuhn (1969). Forma y simetria. -Ed. Editorial Universitaria de Buenos Aires, p. 7–55.
Wolpert, L. (1969). Positional information and the spatial pattern of cellular differentiation. - J. theor. Biol. 25, p. 1–47.
Wolpert, L. (1971). Positional information and pattern formation. - Curr. Topics developm. Biol. 6, p. 183–224.
Wrenn, J. T. & N. K. Wessells (1969). An ultrastructural study of lens invagination in the mouse. - J. exp. Zool. 171, p. 359–368.
Yamada, K. M., B. S. Spooner & N. K. Wessells (1970). Axon growth: roles of microfilaments and microtubules. - Proc. nat. Acad. Sci., U.S.A. 66, p. 1206–1212.
Yamada, K. M., B. S. Spooner & N. K. Wessells (1971). Ultrastructure and function of growth cones and axons of cultured nerve cells. - J. Cell Biol. 49, p. 614–635.
Author information
Authors and Affiliations
Additional information
Fellow of the Consejo Nacional de Investigaciones Cientificas y Tecnicas (CONICET, Argentina).
Rights and permissions
About this article
Cite this article
Herkovits, J., Faber, J. Shape: Its development and regulation capacity during embryogenesis. Acta Biotheor 27, 185–200 (1978). https://doi.org/10.1007/BF00115833
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00115833