Journal of Biosciences

, Volume 17, Issue 3, pp 193–215

Generic physical mechanisms of morphogenesis and pattern formation as determinants in the evolution of multicellular organization

  • Stuart A. Newman


Early embryos of metazoan species are subject to the same set of physical forces and interactions as any small parcels of semi-solid material, living or nonliving. It is proposed that such “generic” properties of embryonic tissues have played a major role in the evolution of biological form and pattern by providing an array of morphological templates, during the early stages of metazoan phylogeny, upon which natural selection could act. The generic physical mechanisms considered include sedimentation, diffusion, and reaction-diffusion coupling, all of which can give rise to chemical nonuniformities (including periodic patterns) in eggs and small multicellular aggregates, and differential adhesion, which can lead to the formation of boundaries of non-mixing between adjacent cell populations. Generic mechanisms that produce chemical patterns, acting in concern with the capacity of cells to modulate their adhesivity (presumed to be a primitive, defining property of metazoa), could lead to multilayered gastrulae of various types, segmental organization, and many of the other distinguishing characteristics of extant and extinct metazoan body plans. Similar generic mechanisms, acting on small tissue primordia during and subsequent to the establishment of the major body plans, could have given rise to the forms of organs, such as the vertebrate limbs. Generic physical processes acting on a single system of cells and cell products can often produce a widely divergent set of morphological phenotypes, and these are proposed to be the raw material of the evolution of form. The establishment of any ecologically successful form by these mechanisms will be followed, under this hypothesis, by a period of genetic evolution, in which the recruitment of gene products to produce the “generically templated” morphologies by redundant pathways would be favoured by intense selection, leading to extensive genetic change with little impact on the fossil record. In this view, the stabilizing and reinforcing functions of natural selection are more important than its ability to effect incremental change in morphology. Aspects of evolution which are problematic from the standard neo-Darwinian viewpoint, or not considered within that framework, but which follow in a straightforward fashion from the view presented here, include the beginnings of an understanding of why organisms have the structure and appearance they’ do, why homoplasy (the recurrent evolution of certain forms) is so prevalent, why evolution has the tempo and mode it does (“punctuated equilibrium”), and why a “rapid” burst of morphological evolution occurred so soon after the origin of the metazoa.


Metazoa origin of form developmental templates 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Ancel P and Vintemberger P 1948 Recherches Sur le Determinism de la Symmetric Bilatérale Dans L’oeuf Des Amphibians;Bull. Biol. France Belg. (Suppl.) 31 1–182Google Scholar
  2. Akam B 1989 Making stripes inelegantly;Nature (London) 341 282–283CrossRefGoogle Scholar
  3. Atchley W R, Newman S and Cowley D E 1988 Genetic divergence in mandible form in relation to molecular divergence in inbred mouse strains;Genetics 120 239–253PubMedGoogle Scholar
  4. Baldwin J M 1902Development and evolution (New York: Macmillan)Google Scholar
  5. Balfour F M 1885 A comparison of the early stages in the development of vertebrates; inThe works of Francis Maitland Balfour (eds) M Foster and A Sedgwick (London: Macmillan) Vol. 1, pp 112–133 (originally published 1875)Google Scholar
  6. Bonner J T 1988The evolution of complexity (Princeton: Princeton University Press)Google Scholar
  7. Buss L 1987The evolution of individuality (Princeton: Princeton University Press)Google Scholar
  8. Castets V, Dulls E, Boissonade J and DeKepper 1990 Experimental evidence of a sustained standing Turing-type nonequilibrium chemical pattern;Phys. Rev. Lett. 64 2953–2956PubMedCrossRefGoogle Scholar
  9. De Gennes P G 1985 Wetting: Statics and dynamics;Rev. Mod. Phys. 57 827–863CrossRefGoogle Scholar
  10. DeLisi C 1988 The human genome project;Am. Sci. 76 488–493Google Scholar
  11. Deuchar E 1975Cellular interactions in animal development (New York: Halstead)Google Scholar
  12. Duellman W E and Trueb L 1986Biology of amphibians (New York: McGraw-Hill)Google Scholar
  13. Elinson R P 1987 Change in developmental patterns: Embryos of amphibians with large eggs; inDevelopment as an evolutionary process (eds) R A Raft and E C Raft (New York: A R Liss) pp 1–21Google Scholar
  14. Elinson R P and Rowning B 1988 A transient array of parallel microtubules in frog eggs: Potential tracks for a cytoplasmic rotation that specifies the dorso-ventral axis;Dev. Biol. 128 185–197PubMedCrossRefGoogle Scholar
  15. Epstein 1 R 1991 Spiral waves in chemistry and biology;Science 252 67PubMedCrossRefGoogle Scholar
  16. Fedonkin M A 1985 Precambrian metazoans: The problems of preservation, systematics and evolution;Philos. Trans. R. Soc. London B311 27–45Google Scholar
  17. Forgacs G, Jaikaria N 8, Frisch H L and Newman S A 1989 Wetting, percolation and morphogenesis in a model tissue system;J. Theor. Biol. 140 417–430PubMedGoogle Scholar
  18. Frasch M and Levine M 1987 Complementary patterns ofeven-skipped andfushi tarazu expression involve their differential regulation by a common set of segmentation genes inDrosophila;Genes Dev. 1981-995Google Scholar
  19. Frasch M, Hoey T, Rushlow C, Doyle H and Levine B 1987 Characterization and localization of theeven-skipped protein of Drosophila; EMBO J. 6 749–759PubMedGoogle Scholar
  20. Friedlander D R, Merge R-M, Cunningham B A and Edelman G M 1989 Cell sorting-out is modulated by both the specificity and amount of different cell adhesion molecules (CABs) expressed on cell surfaces;Proc. Natl. Acad. Sci. USA 86 7043–7047PubMedCrossRefGoogle Scholar
  21. Gierer A and Reinhardt H 1972 A theory of biological pattern formation;Kybernetik 12 30–39PubMedCrossRefGoogle Scholar
  22. Gilbert S F 1991Developmental biology 3rd edition (Sunderland, MA: Sinauer)Google Scholar
  23. Glaessner M F 1984The dawn of animal life (Cambridge: Cambridge University Press)Google Scholar
  24. Goldschmidt R 1938Physiological genetics (New York: McGraw-Hill)Google Scholar
  25. Goto T, MacDonald P and Maniatis T 1989 Early and late periodic patterns ofeven-skipped expression are controlled by distinct regulatory elements that respond to different spatial cues;Cell 57 413–422PubMedCrossRefGoogle Scholar
  26. Gould S J 1977Ontogeny and phylogeny (Cambridge, MA: Harvard University Press)Google Scholar
  27. Gould S J 1989Wonderful life (New York: W W Norton)Google Scholar
  28. Gould S J and Lewontin R C 1979 The spandrels of San Marco and the Panglossian paradigm: A critique of the adaptationist programme;Proc. R. Soc. London B205 581–598CrossRefGoogle Scholar
  29. Gould S J and Eldredge N 1977 Punctuated equilibria: The tempo and mode of evolution reconsidered;Paleobiology3 115–151Google Scholar
  30. Hamburger V and Hamilton H L 1951 A series of normal stages in the development of the chick embryo;J. Morphol. 88 49–92CrossRefGoogle Scholar
  31. Harrison L G and Hillier N A 1985 Quantitative control ofAcetabularia morphogenesis by extracellular calcium: A test of kinetic theory;J. Theory. Biol. 114 177–192CrossRefGoogle Scholar
  32. Heintzelman K F, Phillips H M and Davis G S 1978 Liquid-tissue behavior and differential cohesiveness during chick limb budding;J. Embryol. Exp. Morphol. 47 1–15PubMedGoogle Scholar
  33. Hiller B 1984Ionic channels of excitable membranes (Sunderland, BA: Sinauer)Google Scholar
  34. Hiromi Y and Gehring W J 1987 Regulation and function of theDrosophila segmentation genefushi tarazu; Cell 50 963–974PubMedCrossRefGoogle Scholar
  35. Holtfreter J 1943a Properties and functions of the surface coat m amphibian embryos;J. Exp. Zool. 93 251–323CrossRefGoogle Scholar
  36. Holtfreter J 1943b A study of the mechanics of gastrulation. PartI;J. Exp. Zool. 94 261–318CrossRefGoogle Scholar
  37. Holtfreter J 1944 A study of the mechanics of gastrulation. Part II:J. Exp. Zool. 95 171–212CrossRefGoogle Scholar
  38. Hubbard R 1982 The theory and practice of genetic reductionism —From Mendel’s laws to genetic engineering; inTowards a liberatory biology (ed.) S Rose (London: Allison and Busby) pp 62–78Google Scholar
  39. Hulskamp M, Schröder C, Pfeifle C, Jackle H and Tautz D 1989 Posterior segmentation of theDrosophila embryo in the absence of a maternal posterior organizer gene,Nature (London) 338 629–632CrossRefGoogle Scholar
  40. Ingham P W 1988 The molecular genetics of embryonic pattern formation inDrosophila;Nature (London) 335 25–34CrossRefGoogle Scholar
  41. Irish V, Lehmann R and Akam M 1989 The Drosophila posterior-group gene nanos functions by repressinghunchback activity;Nature (London) 338 646–648CrossRefGoogle Scholar
  42. Johnston T D and Gottlieb G 1990 Neophenogenesis: A developmental theory of phenotypic evolution:J. Theory. Biol. 147 471–495CrossRefGoogle Scholar
  43. Kauffman S A, Shymko R M and Trabert K 1978 Control of sequential compartment formation inDrosophila;Science 199 259–270PubMedCrossRefGoogle Scholar
  44. Lacalli T C and Harrison L G 1978 The regulatory capacity of Turing’s model for morphogenesis, with application to slime moulds;J. Theory. Biol. 70 273–295CrossRefGoogle Scholar
  45. Lacalli T C, Wilkinson D A and Harrison 1. G 1988 Theoretical aspects of stripe formation in relation toDrosophila segmentation;Development 103 105–113Google Scholar
  46. Leonard C M, Fuld H M, Frenz D A, Downie S A, Massague J and Newman S A 1991 Role of transforming growth factor-p in,chondrogenic pattern formation in the developing limb: stimulation of mesenchymal condensation and fibronectin gene expression by exogenous TGF-Β, and evidence for endogenous TGF-Β-like activity;Dev. Biol. 145 99–109PubMedCrossRefGoogle Scholar
  47. Matsuda R 1987Animal changing environments with special reference to abnormal metamorphosis (New York: Wiley)Google Scholar
  48. Maynard Smith J 1968Mathematical ideas in biology (Cambridge: Cambridge University Press)Google Scholar
  49. Meinhardt H 1988 Models for maternally supplied positional information and the activation of segmentation genes inDrosophila embryogenesis;Development (Suppl.) 104 95–110Google Scholar
  50. Mergner H 1971 Cnidaria; inExperimental embryology of marine and fresh water invertebrates (ed.) G Reverberi (New York: Elsevier)Google Scholar
  51. Meyer A, Kocher T D, Basasibwaki P and Wilson A C 1990 Monophyletic origins of Lake Victoria cichlid fishes suggested by mitochondrial DNAsequences;Nature (London) 347 550–553CrossRefGoogle Scholar
  52. Minchin E A 1900 Sponges; inA treatise on zoology (ed.) E R Lankester (London: Adam and Charles Black) part II, p 70Google Scholar
  53. Mittenthal J E 1989 Physical aspects of the organization of development; Complex Systems10 491–528Google Scholar
  54. Needham J 1936Order and life (New Haven: Yale University Press)Google Scholar
  55. Neff A W, Wakahara B, Jurand A and Malacinski G M 1984 Experimental analyses of cytoplasmic rearrangements which follow fertilization and accompany symmetrization of invertedXenopus eggs;J. Embryol. Exp. Morphol. 80 197–224PubMedGoogle Scholar
  56. Newman S A 1984 Vertebrate bones and violin tones: Music and the making of limbs;The Sciences 24 38–43Google Scholar
  57. Newman S A 1988 Idealist biology;Persp. Biol. Med. 31 353–368Google Scholar
  58. Newman S A and Comper W D 1990 ’Generic’ physical mechanisms of morphogenesis and pattern formation;Development 110 I-IGoogle Scholar
  59. Newman S A and Frisch H L 1979 Dynamics of skeletal pattern formation in developing chick limb;Science 205 662–668PubMedCrossRefGoogle Scholar
  60. Newman S A, Frenz D A, Tomasek J J and Rabuzzi D D 1985 Matrix-driven translocation of cells and nonliving particles;Science 228 885–889PubMedCrossRefGoogle Scholar
  61. Newman S A, Frisch H L and Percus J K 1988 On the stationary state analysis of reaction-diffusion mechanisms for biological pattern formation;J. Theor. Biol. 134 183–197PubMedCrossRefGoogle Scholar
  62. Nijhout H F 1990 Metaphors and the role of genes in development;BioEssays 12 441–446PubMedCrossRefGoogle Scholar
  63. Ohio S 1970Evolution by gene duplication (Heidelberg: Springer-Verlag)Google Scholar
  64. Oyama S 1985The ontogeny of information (Cambridge: Cambridge University Press)Google Scholar
  65. Phillips H M and Davis G S 1978 Liquid-tissue mechanics in amphibian gastrulation: Germ-layer assembly inRana pipiens;Am. Zool. 18 81 -93Google Scholar
  66. Raff R A 1987 Constraint, flexibility and phylogenetic history in the evolution of direct development in sea urchins;Dev. Biol. 119 6–19PubMedCrossRefGoogle Scholar
  67. Sanderson M J and Donoghue M J 1989 Patterns of variation in levels of homoplasy;Evolution 43 1781–1795CrossRefGoogle Scholar
  68. Schmalhausen 1 1 1949Factors of evolution (Philadelphia: Blakiston)Google Scholar
  69. Simpson G G 1953 The Baldwin effect;Evolution 7 110–117CrossRefGoogle Scholar
  70. Slack J 1984 A Rosetta stone for pattern formation in animals?:Nature (London) 310 364 365CrossRefGoogle Scholar
  71. Stanojevic D, Holey T and Levine M 1989 Sequence-specific DNA-binding activities of the gap proteins encoded byhunchback andkruppel inDrosophila;Nature (London) 341 331–335CrossRefGoogle Scholar
  72. Steinberg M S 1978 Specific cell ligands and the differential adhesion hypothesis: How do they fit together’?: inSpecificity of embryological interactions (ed.) D R Garrod,London: Chapman and Hall) pp 97–130Google Scholar
  73. Steinberg M S and Poole T J 1982 Liquid behavior of embryonic tissues; inCell behavior (eds) R Bellairs and A S G Curtis (Cambridge: Cambridge University Press) pp 583–607Google Scholar
  74. Stent G S 1985 Thinking in one dimension: The impact of molecular biology on development; Cell40 1–2PubMedCrossRefGoogle Scholar
  75. Thompson D W 1942On growth and form (New York: Cambridge University Press)Google Scholar
  76. Turing A 1952 The chemical basis of morphogenesis;Philos. Trans. R. Soc. London B237 37–72Google Scholar
  77. Vale R D 1987 Intracellular transport using microtubule-based motors;Annu. Rev. Cell Biol. 3 347 378PubMedCrossRefGoogle Scholar
  78. Vincent 3-P, Oster G F and Gerhart J C 1986 Kinematics of gray crescent formation inXenopus eggs: The displacement of subcortical cytoplasm relative to the egg surface;Dev. Biol. 113 484–500PubMedCrossRefGoogle Scholar
  79. Waddington C H 1957The strategy of the genes (London: Allen and Unwin)Google Scholar
  80. Waddington C H 1961The nature of life (London: Allen and Unwin)Google Scholar
  81. Wake D B 1991 Homoplasy: The result of natural selection or evidence of design limitations?;Am. Nat. 138 543–567CrossRefGoogle Scholar
  82. Wake D B and Larson A 1987 Multidimensional analysis of an evolving lineage;Science 238 42–48PubMedCrossRefGoogle Scholar
  83. Watson J D, Hopkins N H Roberts J W, Steitz J A and Weiner A M 1987Molecular biology of the gene 4th edition (Menlo Park, CA: Benjamin/Cummings)Google Scholar
  84. Webster G and Goodwin B 1982 History and structure in biology; inTowards a liberatory biology (ed.) S Rose (London: Allison and Busby) pp 103–119Google Scholar
  85. Whittington H B 1985The Burgess Shale (New Haven: Yale University Press)Google Scholar
  86. Wolpert L 1969 Positional information and spatial pattern of cellular differentiation;J. Theor. Biol. 25 1–47PubMedCrossRefGoogle Scholar
  87. Wright B e. and Davison B F 1980 Mechanisms of development and aging;Mech. Ageing Dev. 12 213–219PubMedCrossRefGoogle Scholar

Copyright information

© Indian Academy of Sciences 1992

Authors and Affiliations

  • Stuart A. Newman
    • 1
  1. 1.Department of Cell Biology and AnatomyNew York Bedical CollegeValhallaUSA

Personalised recommendations