Biological Theory

, Volume 2, Issue 4, pp 349–359 | Cite as

Collectivity in Context: Modularity, Cell Sociology, and the Neural Crest



Modularity has become a central and remarkably useful concept in evolutionary developmental biology, offering an explanation of how independent, interacting units make possible developmental events and evolutionary changes. These modules exist at several different levels of organization, from genes to signal transduction pathways to cell populations. Cell populations, which are multicellular modules, provide an opportunity both to clarify our notion of modularity and to reexamine such central concepts as cell-to-cell communication. Rosine Chandebois’s work on “cell sociology” is reframed in the language of modularity in order to show how groups of cells maintain their collective identity during development and how signaling information from the group’s environment is received by the constituent cells. In a “test case” for our account of multicellular modules, we consider the vertebrate neural crest, a migratory cell population made up of several subpopulations. The neural crest proves yet again to be a complex case, showing the importance of taking into account both developmental and evolutionary transformations of multicellular modules.


cell-cell signaling EvoDevo homoiogenetic induction modularity neural crest pleiotropy 


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  1. Atchley WR, Hall BK (1991) A model for development and evolution of complex morphological structures. Biological Reviews of the Cambridge Philosophical Society 66: 101–157.CrossRefGoogle Scholar
  2. Baatz M, Wagner GP (1997) Adaptive inertia caused by hidden pleiotropic effects. Theoretical Population Biology 51: 49–66.CrossRefGoogle Scholar
  3. Bannerman P, Nichols W, Puhalla S, Oliver T, Berman M, Pleasure D (2000) Early migratory rat neural crest cells express functional gap junctions: Evidence that neural crest cell survival requires gap junctions function. Journal of Neuroscience Research 61: 605–615.CrossRefGoogle Scholar
  4. Blazquez MALN, Soowai IL, Weigel D (1997) LEAFY expression and flower initiation in Arabidopsis. Development 124: 3835–3884.Google Scholar
  5. Bolker JA (2000) Modularity in development and why it matters to evo-devo. American Zoologist 40: 770–776.CrossRefGoogle Scholar
  6. Bonner JT (1988) The Evolution of Complexity by Means of Natural Selection. Princeton, NJ: Princeton University Press.Google Scholar
  7. Brandon RN (1999) The units of selection revisited: The modules of selection. Biology and Philosophy 14: 167–180.CrossRefGoogle Scholar
  8. Carroll SB, Grenier JK, Weatherbee RD (2005) From DNA to Diversity: Molecular Genetics and the Evolution of Animal Design, 2nd ed. Malden, MA: Blackwell.Google Scholar
  9. Chandebois R (1983) Automation in Animal Development: A New Theory Derived from the Concept of Cell Sociology (Faber J, trans). Monographs in Developmental Biology, Vol. 16. Basel: Karger.Google Scholar
  10. Clearwater MJ, Gould KS (1994) Comparative leaf development of juvenile and adult Pseudopanax crassifolius. Canadian Journal of Botany 72: 658–670.CrossRefGoogle Scholar
  11. Davidson EH (2006) The Regulatory Genome: Gene Regulatory Networks in Development and Evolution. Burlington, MA: Elsevier/Academic Press.Google Scholar
  12. Dover G (2000) How genomic and developmental dynamics affect evolutionary processes. BioEssays 22: 1153–1159.CrossRefGoogle Scholar
  13. Emlen DJ, Hunt J, Simmons LW (2005) Evolution of sexual dimorphism and male dimorphism in the expression of beetle horns: Phylogenetic evidence for modularity, evolutionary lability, and constraint. American Naturalist 166: S42–S68.CrossRefGoogle Scholar
  14. Franz-Odendaal TA, Hall BK (2006) Modularity and sense organs in the blind cavefish, Astyanax mexicanus. Evolution and Development 8: 94–100.CrossRefGoogle Scholar
  15. Gass GL, Bolker JA (2003) Modularity. In: Key Concepts and Approaches in Evolutionary Developmental Biology (Hall BK, Olson WM, eds), 260–267. Cambridge, MA: Harvard University Press.Google Scholar
  16. Gerhart J (1997) In memoriam Pieter D. Nieuwkoop (1917–1996). Developmental Biology 182: 1–4.CrossRefGoogle Scholar
  17. Gilbert SF (2000) Developmental Biology, 6th ed. Sunderland, MA: Sinauer.Google Scholar
  18. Gilbert SF (2001) Ecological developmental biology: Developmental biology meets the real world. Developmental Biology 233: 1–12.CrossRefGoogle Scholar
  19. Gilbert SF, Bolker, JA (2001) Homologies of process and modular elements of embryonic construction. Journal of Experimental Zoology (Molecular and Developmental Evolution) 291: 1–12.CrossRefGoogle Scholar
  20. Gilbert SF, Opitz JM, Raff RA (1996) Resynthesizing evolutionary and developmental biology. Developmental Biology 173: 357–372.CrossRefGoogle Scholar
  21. Griswold CL (2006) Pleiotropic mutation, modularity and evolvability. Evolution and Development 8: 81–93.CrossRefGoogle Scholar
  22. Gurdon JB (1988) A community effect in animal development. Nature 336: 772–774.CrossRefGoogle Scholar
  23. Gurdon JB (1989) The localization of an inductive response. Development 105: 27–33.Google Scholar
  24. Gurdon JB, Lemaire P, Kato K (1993) Community effects and related phenomena in development. Cell 75: 831–834.CrossRefGoogle Scholar
  25. Hall BK (1997) Germ layers and the germ-layer theory revisited: Primary and secondary germ layers, neural crest as a fourth germ layer, homology, demise of the germ-layer theory. Evolutionary Biology 30: 121–186.Google Scholar
  26. Hall BK (1999) The Neural Crest in Development and Evolution. New York: Springer-Verlag. (Second edition in preparation.)CrossRefGoogle Scholar
  27. Hall BK (2000) The neural crest as a fourth germ layer and vertebrates as quadroblastic not triploblastic. Evolution &Development 2: 1–3.CrossRefGoogle Scholar
  28. Hall BK (2001) The gene is not dead, merely orphaned and seeking a home. Evolution & Development 3: 225–228.CrossRefGoogle Scholar
  29. Hall BK (2005a) Consideration of the neural crest and its skeletal derivatives in the context of novelty/innovation. Journal of Experimental Zoology (Molecular and Developmental Evolution) 304B: 548–557.CrossRefGoogle Scholar
  30. Hall BK (2005b) Bones and Cartilage: Developmental and Evolutionary Skeletal Biology. London: Elsevier Academic Press.Google Scholar
  31. Hallgrímsson B, Hall BK, eds (2005) Variation: A Central Concept in Biology. New York: Elsevier/Academic Press.Google Scholar
  32. Hartwell LH, Hopfield JJ, Leibler S, Murray AW (1999) From molecular to modular cell biology. Nature 402: C47–C52.CrossRefGoogle Scholar
  33. Jacob F (1977) Evolution and tinkering. Science 196: 1161–1166.CrossRefGoogle Scholar
  34. Jacobson M (1991) Developmental Neurobiology, 3rd ed. New York: Plenum Press.CrossRefGoogle Scholar
  35. Kirby ML (1988) Nodose placode provides ectomesenchyme to the developing chick heart in the absence of cardiac neural crest. Cell and Tissue Research 252: 17–22.CrossRefGoogle Scholar
  36. Kirby ML (1989) Plasticity and predetermination of mesencephalic and trunk neural crest transplanted into the region of the cardiac neural crest. Developmental Biology 134: 402–412.CrossRefGoogle Scholar
  37. Krull CE, Lansford R, Gale NW, Collazo A, Marcelle C, Yancopoulos GD, Fraser SE, Bronner-Fraser M (1997) Interactions of Eph-related receptors and ligands confer rostrocaudal pattern to trunk neural crest migration. Current Biology 1: 572–580.Google Scholar
  38. Lande R, Arnold SJ (1983) The measurement of selection on correlated characters. Evolution 37: 1210–1226.CrossRefGoogle Scholar
  39. Lewontin RC (1970) The units of selection. Annual Reviews in Ecology and Systematics 1: 1–18.CrossRefGoogle Scholar
  40. Lewontin RC (1978) Adaptation. Scientific American 239: 212–228.CrossRefGoogle Scholar
  41. Maclean N, Hall BK (1987) Cell Commitment and Differentiation. Cambridge: Cambridge University Press.Google Scholar
  42. Moss L (2001) Deconstructing the gene and reconstructing molecular developmental systems. In: Cycles of Contingency: Developmental Systems and Evolution (Oyama S, Griffiths PE, Gray RD, eds), 85–97. Cambridge, MA: MIT Press.Google Scholar
  43. Moss L (2003) What Genes Can’t Do. Cambridge, MA: MIT Press.Google Scholar
  44. Müller GB, Wagner GP (2003) Innovation. In: Keywords & Concepts in Evolutionary Developmental Biology (Hall BK, Olson WM, eds), 218–227. Cambridge, MA: Harvard University Press.Google Scholar
  45. Nakagawa S, Takeichi M (1998) Neural crest emigration from the neural tube depends on regulated cadherin expression. Development 125: 2963–2971.Google Scholar
  46. Raff RA (1996) The Shape of Life: Genes, Development, and the Evolution of Animal Form. Chicago: University of Chicago Press.Google Scholar
  47. Raff RA, Sly BJ (2000) Modularity and dissociation in the evolution of gene expression territories in development. Evolution and Development 2: 102–113.CrossRefGoogle Scholar
  48. Ravasz E, Somera AL, Mongru DA, Oltvai ZN, Barabasi A-L (2002) Hierarchical organization of modularity in metabolic networks. Science 297: 1551–1555.CrossRefGoogle Scholar
  49. Stern DL (2000) Perspective: Evolutionary developmental biology and the problem of variation. Evolution 54: 1079–1091.CrossRefGoogle Scholar
  50. Stone JR, Hall BK (2004) Latent homologues for the neural crest as an evolutionary novelty. Evolution and Development 6: 123–129.CrossRefGoogle Scholar
  51. Trainor PA, Melton KR, Manzanares M (2003) Origins and plasticity of neural crest cells and their roles in jaw and craniofacial skeleton. International Journal of Developmental Biology 47: 541–553.Google Scholar
  52. Vaglia JL, Hall BK (1999) Regulation of neural crest cell populations in vertebrates: Occurrence, distribution and underlying mechanisms. International Journal of Developmental Biology 43: 95–110.Google Scholar
  53. Vaglia JL, Hall BK (2000) Patterns of migration and regulation of trunk neural crest cells in zebrafish (Danio rerio). International Journal of Developmental Biology 44: 867–881.Google Scholar
  54. Vickaryous M, Hall BK (2006) Human cell type diversity, evolution development classification with special reference to cells derived from the neural crest. Biological Reviews of the Cambridge Philosophical Society 81: 425–455.CrossRefGoogle Scholar
  55. von Dassow G, Munro E (1999) Modularity in animal development and evolution: Elements of a conceptual framework for EvoDevo. Journal of Experimental Zoology (Molecular and Developmental Evolution) 285: 307–325.CrossRefGoogle Scholar
  56. Wagner GP (1996) Homologues, natural kinds, and the evolution of modularity. American Zoologist 36: 36–43.Google Scholar
  57. Wagner GP, Altenberg L (1996) Complex adaptations and the evolution of evolvability. Evolution 50: 967–976.CrossRefGoogle Scholar
  58. Waldo KL, Lo CW, Kirby ML (1999) Connexin 43 expression reflects neural crest patterns during cardiovascular development. Developmental Biology 208: 307–323.CrossRefGoogle Scholar
  59. Wilkins AS (2002) The Evolution of Developmental Pathways. Sunderland, MA: Sinauer.Google Scholar
  60. Wilson RA (1999) Realism, essence, and kind: Resuscitating species essentialism? In: Species: New Interdisciplinary Essays (Wilson RA, ed), 187–207. Cambridge, MA: MIT Press.Google Scholar

Copyright information

© Konrad Lorenz Institute for Evolution and Cognition Research 2008

Authors and Affiliations

  1. 1.Department of BiologyDalhousie UniversityHalifaxCanada

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