Biology & Philosophy

, Volume 22, Issue 4, pp 579–601 | Cite as

The uniqueness of biological self-organization: challenging the Darwinian paradigm

Original Paper

Abstract

Here we discuss the challenge posed by self-organization to the Darwinian conception of evolution. As we point out, natural selection can only be the major creative agency in evolution if all or most of the adaptive complexity manifest in living organisms is built up over many generations by the cumulative selection of naturally occurring small, random mutations or variants, i.e., additive, incremental steps over an extended period of time. Biological self-organization—witnessed classically in the folding of a protein, or in the formation of the cell membrane—is a fundamentally different means of generating complexity. We agree that self-organizing systems may be fine-tuned by selection and that self-organization may be therefore considered a complementary mechanism to natural selection as a causal agency in the evolution of life. But we argue that if self-organization proves to be a common mechanism for the generation of adaptive order from the molecular to the organismic level, then this will greatly undermine the Darwinian claim that natural selection is the major creative agency in evolution. We also point out that although complex self-organizing systems are easy to create in the electronic realm of cellular automata, to date translating in silico simulations into real material structures that self-organize into complex forms from local interactions between their constituents has not proved easy. This suggests that self-organizing systems analogous to those utilized by biological systems are at least rare and may indeed represent, as pre-Darwinists believed, a unique ascending hierarchy of natural forms. Such a unique adaptive hierarchy would pose another major challenge to the current Darwinian view of evolution, as it would mean the basic forms of life are necessary features of the order of nature and that the major pathways of evolution are determined by physical law, or more specifically by the self-organizing properties of biomatter, rather than natural selection.

Keywords

Self-organization Cumulative selection Unique hierarchy of natural forms Contingency Necessity Robustness Pre-Darwinian 

References

  1. Agassiz L (1874) Evolution and the permanence of type. Atlantic Monthly 33:92–101Google Scholar
  2. Anfinsen CB (1973) Principles that govern the folding of protein chains. Science 181:223–230Google Scholar
  3. Bak P (1996) How nature works: the science of self-organized criticality. Springer Verlag, NYGoogle Scholar
  4. Ball P (1999) The self-made tapestry: pattern formation in nature. Oxford University Press, OxfordGoogle Scholar
  5. Barth JV, Costantini G, Kern K (2005) Engineering atomic and molecular nanostructures at surfaces. Nature 237:671–679Google Scholar
  6. Bornens M (1991) Cell polarity: intrinsic or externally imposed? New Biol 3:627–636Google Scholar
  7. Brandon C, Tooze J (1999) Introduction to protein structure. Garland Publishing Inc., NYGoogle Scholar
  8. Brooks RA (2001) The relationship between matter and life. Nature 409:409–411Google Scholar
  9. Camazine S, Deneubourg J-L, Franks NR, Theraulaz G, Bonabeau E (2001) Self-organization in biological systems. Princeton University Press, PrincetonGoogle Scholar
  10. Chambers R (1844) Vestiges of the natural history of creation. John Churchill, LondonGoogle Scholar
  11. Chivian D, Robertson T, Bonneau R, Baker D (2003) Ab initio methods. In: Bourne E, Weissig H (eds) Structural informatics. Wiley, NY, pp 547–557Google Scholar
  12. Cherdantseva EM, Cherdantsev VG (2006) Geometry and mechanics of teleost gastrulation and the formation of primary body axes. Int J Dev Biol 50:157–168Google Scholar
  13. Conway Morris S (2003) Life’s solution: inevitable humans in a lonely universe. Cambridge University Press, CambridgeGoogle Scholar
  14. Csete ME, Doyle JC (2002) Reverse engineering of biological complexity. Science 295:1164–1669Google Scholar
  15. Darwin C (1872) The origin of species. John Murray, LondonGoogle Scholar
  16. Dawkins R (1976) The selfish gene. Oxford University Press, OxfordGoogle Scholar
  17. Dawkins R (1986) The blind watchmaker, Longman Scientific and Technical, UKGoogle Scholar
  18. Dawkins R (1996) Climbing mount improbable. W. W. Norton, NYGoogle Scholar
  19. Dawkins R (2004) The ancestor’s tale. Weidenfeld and Nicholson, LondonGoogle Scholar
  20. Deacon T (1997) The symbolic species. Penguin Books, LondonGoogle Scholar
  21. Denton MJ, Marshall CJ (2001) The laws of form revisited. Nature 410:417Google Scholar
  22. Denton MJ, Marshall CJ, Legge M (2002) The protein folds as platonic forms: new support for the Pre-Darwinian conception of evolution by natural law. J Theor Biol 219:325–342Google Scholar
  23. Dennett D (1995) Darwin’s dangerous idea. Simon and Schuster, NYGoogle Scholar
  24. Depew DJ, Weber BH (1988) Consequences of nonequilibrium thermodynamics for the Darwinian tradition. In: Weber BH, Depew DJ, Smith JD (eds) Entropy, information and evolution: new perspectives on physical and biological evolution. MIT press, Cambridge, Mass, pp 316–354Google Scholar
  25. Drexler KE (1986) Engines of creation. Anchor Books, NYGoogle Scholar
  26. Driesch H (1929) The science and philosophy of the organism. A. and C. Black, LondonGoogle Scholar
  27. Edelman GM (1987) Neural Darwinism. Basic Books, NYGoogle Scholar
  28. Florey J (1969) Statistical mechanics of chain molecules. Wiley, NYGoogle Scholar
  29. Franks NR, Wilby A, Silverman BW, Tofts C (1992) Self-organizing nest construction in ants: sophisticated building by blind bulldozing. Anim Behav 44:357–375Google Scholar
  30. Gale B (1972) The Darwinian concept of the struggle for existence. ISIS 63:321–344Google Scholar
  31. Gardner R, Surani M, Solter D (2003) Epigenesis versus preformation during mammalian development. Phil Trans R Soc Lond B 358:1313–1315Google Scholar
  32. Gleick J (1998) Chaos. Vintage Press, LondonGoogle Scholar
  33. Green JBA, Dominguez I, Davidson LA (2004) Self organization of vertebrate mesoderm based on simple boundary conditions. Dev Dynam 231:576–581Google Scholar
  34. Gribben J (2005) Deep simplicity. Penguin Books, LondonGoogle Scholar
  35. Goodwin BC (1994) How the leopard changed its spots. Charles Scribner, NYGoogle Scholar
  36. Gould SJ (1989) Wonderful life: the Burgess shale and the nature of history. W. W. Norton, NYGoogle Scholar
  37. Gould SJ (2002) The structure of evolutionary theory. Harvard University Press, Cambridge, MassGoogle Scholar
  38. Haken H (1977) Synergetics: an introduction. Nonequilibrium phase transitions and self-organization in physics chemistry and biology. Springer Verlag, NYGoogle Scholar
  39. Harold FM (2001) The way of the cell. Oxford University Press, NYGoogle Scholar
  40. Holldobler B, Wilson EO (1990) The ants. Harvard University Press, MassGoogle Scholar
  41. Huttner WB, Schmidt AA (2002) Membrane curvature: a case of ‘endofeelin’. Trends Cell Biol 12:155–158Google Scholar
  42. Johnson M (1997) Developmental cognitive neuroscience: an introduction. Blackwell, OxfordGoogle Scholar
  43. Kalthoff K (1996) Analysis of biological development. McGraw-Hill, NYGoogle Scholar
  44. Karmiloff-Smith A (1992) Beyond modularity: a developmental perspective on cognitive science. MIT Press, Cambridge, MassGoogle Scholar
  45. Karmiloff-Smith A (2001) Why babies brains are not swiss army knives. In: Rose S, Rose H (eds) Alas Poor Darwin. Vintage, London, pp 144–156Google Scholar
  46. Keller EF (2000) The century of the gene. Harvard University Press, Cambridge, MassGoogle Scholar
  47. Keller R, Davidson L, Shook D (2003) How we are shaped: the biomechanics of gastrulation. Differentiation 7:171–205Google Scholar
  48. Kitano H (2002) Systems biology: a brief overview. Science 295:1662–1664Google Scholar
  49. Kirschner M, Gerhard J (1998) Evolvability. PNAS US 95:8420–8427Google Scholar
  50. Kirschner M, Mitchinson T (1986) Beyond self-assembly: from microtubules to morphogenesis. Cell 45:329–342Google Scholar
  51. Kauffman SA (1993) The origins of order. Oxford University Press, NYGoogle Scholar
  52. Kauffman SA (2000) Investigations. Oxford University Press, NYGoogle Scholar
  53. Kurzweil R (2005) The singularity is near. Viking, NYGoogle Scholar
  54. Langton CG (1989) Artificial life. Addison-Wesley, Redwood City, CaliforniaGoogle Scholar
  55. Lehn J-M (2002) Towards self-organization and complex matter. Science 295:2400–2403Google Scholar
  56. Levy S (1993) The quest for a new creation. Penguin Books, LondonGoogle Scholar
  57. Lewin R (1992) Complexity. Macmillan Press, NYGoogle Scholar
  58. Lipson N, Pollack JB (2000) Automatic design and manufacture of robotic life forms. Nature 406:974–978Google Scholar
  59. Maynard Smith J, Szathmary E (1999) The origins of life: from the birth of life to the origin of language. Oxford University Press, OxfordGoogle Scholar
  60. Maynard Smith J (1992) Taking a chance on evolution. New York Rev Books 14:34–36Google Scholar
  61. Mayr E (2001) What evolution is. Basic Books, NYGoogle Scholar
  62. Miller K (1999) Finding Darwin’s God. Cliff St Books, NYGoogle Scholar
  63. Misteli T (2001) The concept of self-organization in cellular architecture. J Cell Biol 155:181–185Google Scholar
  64. Mitchinson TJ (1992) Self-organization of polymer–motor systems in the cytoskeleton. Trans R Soc Lond B Biol Sci 336:99–106Google Scholar
  65. Monod J (1972) Chance and necessity. Collins, LondonGoogle Scholar
  66. Morowitz HJ (2002) The emergence of everything. Oxford University Press, NYGoogle Scholar
  67. Motosugi N, Bauer T, Polanski Z, Solter D, Hiiragi T (2005) Polarity of mouse embryo is established at blastocyst and is not prepatterned. Genes Dev 19:1081–1092Google Scholar
  68. Nedelec FJ, Surrey T, Maggs AC, Liebler S (1997) Self-organization of microtubules and motors. Nature 389:305–308Google Scholar
  69. Newman SA (1993) Is segmentation generic? BioEssays 15:277–283Google Scholar
  70. Newman SA (1994) Generic physical mechanisms of tissue morphogenesis: a common basis for development and evolution. J Evol Biol 7:467–488Google Scholar
  71. Newman SA (2002) Developmental mechanisms: putting genes in their place. Bioscience 27:97–104Google Scholar
  72. Nijhout HF (1990) Metaphors and the role of genes in development. Bioessays 12:441–446Google Scholar
  73. Nijhout FH (1999) When developmental pathways diverge. PNAS US 96:5348–5350Google Scholar
  74. Owen R (1849) On the nature of limbs. Jan Van Voorst, LondonGoogle Scholar
  75. Owen R (1866) Anatomy of vertebrates. Longmans and Green, LondonGoogle Scholar
  76. Popper K (1965) Conjectures and refutations. Harper Row, NYGoogle Scholar
  77. Przytycka T, Aurora R, Rose GD (1999) A protein taxonomy based on secondary structure. Nat Struct Biol 6:672–682Google Scholar
  78. Ridley M (1997) Evolution. Oxford University Press, OxfordGoogle Scholar
  79. Ridley M (2004) Nature via Nurture. Harper Perennial, LondonGoogle Scholar
  80. Rothemund WK (2006) Folding DNA to create nano shapes and patterns. Nature 440:297–302Google Scholar
  81. Rupke NA (1994) Richard Owen. Yale University Press, New HavenGoogle Scholar
  82. Ruse M (2003) Darwin and design: does evolution have a purpose? Harvard University Press, Cambridge, MassGoogle Scholar
  83. Russell ES (1916) Form and function. John Murray, LondonGoogle Scholar
  84. Salazar-Ciudad I, Newman SA, Sole RV (2001a) Phenotypic and dynamical transitions in model genetic networks I: emergence of patterns and genotype–phenotype relationships. Evol Dev 3:84–94Google Scholar
  85. Salazar-Ciudad I, Sole RV, Newman SA (2001b) Phenotypic and dynamical transitions in model genetic networks II: application to the evolution of segmentation mechanisms. Evol Dev 3:95–103Google Scholar
  86. Salthe SN (1993) Development in evolution:complexity and change in biology. MIT Press, Cambridge, MassGoogle Scholar
  87. Schwann T (1847) Microscopical researches, English translation by Henry Smith, [original published in German in 1839]. Sydenham Society, LondonGoogle Scholar
  88. Shatz CJ (1996) Emergence of order in visual system development. PNAS US 93:602–608Google Scholar
  89. Singer SJ, Nicholson GI (1972) The fluid mosaic model of the cell membrane. Science 175:720–731Google Scholar
  90. Soltor D, Knowles BB (1999) Spatial and temporal control of maternal message. In: Russo VEA et al. (eds) Development. Springer Verlag, Heidelberg, pp 389–394Google Scholar
  91. Srinivasan R, Rose GD (2002) Ab Initio prediction of protein structure using LINUS. Proteins Struct Funct Genet 47:489–495Google Scholar
  92. Strogatz SH (1994) Non linear dynamics and chaos. Perseus Books, NYGoogle Scholar
  93. Surrey T, Nedelec F, Liebler S, Karsenti E (2001) Physical properties determining self-organization of motors and microtubules. Science 292:1167–1171Google Scholar
  94. Trinkaus JP (1984) Cells into organs. Prentice-Hall, NYGoogle Scholar
  95. von Dassow G, Meir E, Munro EM, Odell GM (2000) The segment polarity network is a robust developmental module. Nature 406:188–192Google Scholar
  96. Van Oudenaarden A, Theriot JA (1999) Symmetry breaking by actin polymerization in a model for cell motility. Nat Cell Biol 1:493–499Google Scholar
  97. Waddington CH (1962) New patterns in genetics and development. Columbia University Press, NYGoogle Scholar
  98. Weber B.H (1998) Emergence of life and biological selection from the perspective of complex systems dynamics. In: Van de Vijver G, Salthe SN, Delpos M (eds) Evolutionary systems: biological and epistemological perspectives on selection and self-organization. Kluwer, Dordrecth, pp 59–66Google Scholar
  99. Weber BH, Depew DJ (1996) Natural selection and self-organization: dynamical models as a clue to a new evolutionary synthesis. Biol Philos 11:33–65Google Scholar
  100. Webster G, Goodwin BC (1982) The origin of species: a structuralist approach. J Social Struct 5:15–47Google Scholar
  101. Wiley EO, Brooks DR (1982) Victims of history: a non equilibrium approach to evolution. Syst Zool 31:1–24Google Scholar
  102. Weismann A (1902) The evolution theory. Edward Arnold, LondonGoogle Scholar
  103. Wicken JS (1986) Entropy and evolution: ground rules for discourse. Syst Zool 35:22–36Google Scholar
  104. Wicken JS (1987) Evolution, thermodynamics and information: extending the Darwinian paradigm. Oxford University Press, NYGoogle Scholar
  105. Williams G (1966) Adaptation and natural selection. Oxford University Press, NYGoogle Scholar
  106. Whitesides GM, Grzybowski B (2002) Self-assembly at all scales. Science 295:2418–2421Google Scholar
  107. Wolfram S (2002) A new kind of science. Wolfram Media Inc., Champaign IllinoisGoogle Scholar
  108. Woolfson A (2000) Life without genes. Harper Collins, LondonGoogle Scholar
  109. Yates FE, Garfinkel AW, Yates GB (1987) Self-organizing systems: the emergence of order. Plenum Press, NYGoogle Scholar

Copyright information

© Springer Science+Business Media, B.V. 2006

Authors and Affiliations

  1. 1.Theology Faculty, Harris Manchester CollegeUniversity of OxfordOxfordUK
  2. 2.Department of BiosciencesCOMSATS Institute of Information TechnologyIslamabadPakistan

Personalised recommendations