Theory in Biosciences

, Volume 121, Issue 1, pp 1–80 | Cite as

Modularity and the units of evolution



While many developmental processes (e. g., gene networks or signaling pathways) are astonishingly conserved during evolution, they may be employed differently in different metazoan taxa or may be used multiply in different contexts of development. This suggests that these processes belong to building blocks or modules, viz., highly integrated parts of the organism, which develop and/or function relatively independent from other parts. Such modules may be relatively easy to dissociate from other modules and, therefore, could also serve as units of evolution. However, in order to further explore the implications of modularity for evolution, the vague notion of “modularity” as well as its relation to concepts like “unit of evolution” need to be more precisely specified. Here, a module is characterized as a certain type of dynamic pattern of couplings among the constituents of a process. It may or may not form a spatially contiguous unit. A unit of selection is defined as a unit of those constituents of a reproducing process/system, which exists in different variants and acts as a non-decomposable unit of fitness and variant reproduction during a particular selection process. The more general notion of a unit of evolution is characterized as a nondecomposable unit of constituents with reciprocal fitness dependence, be it due to fitness epistasis or due to the lack of independent variability. Because such fitness dependence may only be observed for some combinations of variants, several constituents may act as a unit of evolution only with a certain probability (coevolution probability). It is argued, that under certain conditions modules are likely to act as units of evolution with high coevolution probabilities, because there is likely to be a close tie between the pattern of couplings of the constituents of a reproducing system and their interdependent fitness contributions. Moreover and contrary to the traditional dichotomy of genes versus organisms as units of selection, modules tend to be more important in delimiting actual units of selection than either organisms or genes, because they are less easily disrupted by recombination than organisms, while having less contextsensitive fitness values than genes. Finally, it is suggested that the evolution of modularity is self-reinforcing, because the flexibility of intermodular connections facilitates the recombination among modules and their multiple employment in new contexts.

Key words

unit of selection epistasis constraints coevolution development evolvability mosaic evolution 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Abeles, M., Prut, Y., Bergman H., Vaardia, E. (1994) Synchronization in neuronal transmission and its importance for information processing. Progress Brain Res. 102: 395–404.CrossRefGoogle Scholar
  2. Abouheif, E. (1997) Developmental genetics and homology: a hierarchical approach. Trend. Ecol. Evol. 12: 405–408.Google Scholar
  3. Alberch, P. (1980) Ontogenesis and morphological diversification. Am. Zool. 20: 653–667.Google Scholar
  4. Altenberg, L. (1995) Genome growth and the evolution of the genotype-phenotype map. In: Banzhaf, W., Eeckman, F. H. (eds) Evolution and biocomputation. Springer, Berlin, pp. 205–259.Google Scholar
  5. Ancel, L. W., Fontana, W. (2000) Plasticity, evolvability and modularity in RNA. J. Exp. Zool. (Mol.Dev.Evol.) 288: 242–283.Google Scholar
  6. Andrews, J. H. (1998) Bacteria as modular organisms. Annu. Rev. Microbiol. 52: 105–126.PubMedGoogle Scholar
  7. Arnone, M. I., Davidson, E. H. (1997) The hardwiring of development: organization and function of genomic regulatory systems. Development 124: 1851–1864.PubMedGoogle Scholar
  8. Artavanis-Tsakonas, S., Rand, M. D., Lake, R. J. (1999) Notch signaling: Cell fate control and signal integration in development. Science 284: 770–776.PubMedGoogle Scholar
  9. Arthur, W. (1997) The origin of animal body plans. Cambridge University Press, Cambridge.Google Scholar
  10. Barton, N. H., Charlesworth, B. (1998) Why sex and recombination? Science 281: 1986–1990.PubMedGoogle Scholar
  11. Beatus, P., Lendahl, U. (1998) Notch and neurogenesis. J. Neurosci. Res. 54: 125–136.PubMedGoogle Scholar
  12. Bernstein, H., Byerly, H. C., Hopf, F. A., Michod, R. E., Vemulapalli, G. K. (1983) The Darwinian dynamic. Quart. Rev. Biol. 58: 185–207.Google Scholar
  13. Bhalla, U. S., Iyengar, R. (1999) Emergent properties of networks of biological signaling pathways. Science 283: 381–387.PubMedGoogle Scholar
  14. Boeke, J. D., Pickeral, O. K. (1999) Retroshuffling the genomic deck. Nature 398: 108–111.PubMedGoogle Scholar
  15. Bolker, J. A., Raff, R. A. (1996) Developmental genetics and traditional homology. Bioessays 18: 489–494.PubMedGoogle Scholar
  16. Bonner, J. T. (1988) The evolution of complexity. Princeton Univ. Press, Princeton.Google Scholar
  17. Brandon, R. N. (1990) Adaptation and environment. Princeton Univ. Press, Princeton.Google Scholar
  18. Brandon, R. N. (1999) The units of selection revisited: the modules of selection. Biology and Philosophy 14: 167–180.Google Scholar
  19. Bray, D. (1995) Protein molecules as computational elements in living cells. Nature 376: 307–312.PubMedGoogle Scholar
  20. Bryant, E. H., McCommas, S. A., Combs, L. M. (1986) The effect of an experimental bottleneck upon quantitative genetic variation in the housefly. Genetics 114: 1191–1211.PubMedGoogle Scholar
  21. Burstein, Z. (1996). A network model of developmental gene hierarchy. J. Theor. Biol. 174: 1–11.Google Scholar
  22. Buss, L. W. (1987) The evolution of individuality. Princeton Univ. Press, Princeton.Google Scholar
  23. Cheverud, J. M. (1984) Quantitative genetics and developmental constraints on evolution by selection. J. Theor. Biol. 110: 155–171.PubMedGoogle Scholar
  24. Cheverud, J. M. (1996) Developmental integration and the evolution of pleiotropy. Am. Zool. 36: 44–50.Google Scholar
  25. Cheverud, J. M., Routman, E. J. (1995) Epistasis and its contribution to genetic variance components. Genetics 139: 1455–1461.PubMedGoogle Scholar
  26. Cheverud, J. M., Vaughn, T. T., Pletscher, L. S., King-Ellison, K., Bailiff, J., Adams, E., Erickson, C., Bonislawski, A. (1999) Epistasis and the evolution of additive genetic variance in populations that pass through a bottleneck. Evolution 53: 1009–1018.Google Scholar
  27. Clarke, B. S., Mittenthal, J. E. (1992) Modularity and reliability in the organization of organisms. Bull. Math. Biol. 54: 1–20.Google Scholar
  28. Conrad, M. (1990) The geometry of evolution. Biosystems 24: 61–81.PubMedGoogle Scholar
  29. Coveney, P., Highfield, R. (1995) Frontiers of complexity. Fawcett Columbina, New York.Google Scholar
  30. Coyne, J. A., Barton, N. H., Turelli, M. (1997) A critique of Sewall Wright’s shifting balance theory of evolution. Evolution 51: 643–671.Google Scholar
  31. Crow, J. F., Engels, W. R., Denniston, C. (1990) Phase three of Wright’s shifting balance theory. Evolution 44: 233–247.Google Scholar
  32. Darwin, C. (1859) On the origin of species. Murray, London.Google Scholar
  33. Davidson, E. H., Peterson, K. J., Cameron, R. A. (1995) Origin of bilaterian body plans: Evolution of developmental regulatory mechanisms. Science 270: 1319–1325.PubMedGoogle Scholar
  34. Dawkins, R. (1976) The selfish gene. Oxford Univ. Press, Oxford.Google Scholar
  35. Dawkins, R. (1978) Replicator selection and the extended phenotype. Zeitschr. Tierpsychol. 47: 61–76.Google Scholar
  36. Dawkins, R. (1982) The extended phenotype. Oxford Univ. Press, Oxford.Google Scholar
  37. Dawkins, R. (1996) Climbing Mount Improbable. Norton, New York.Google Scholar
  38. Dickinson, W. J. (1995) Molecules and morphology: Where’s the homology. Trends Genet. 11: 119–121.PubMedGoogle Scholar
  39. Doolittle, W. F. (1999) Lateral genomics. Trends Genet. 15: M 5-M 8.Google Scholar
  40. Doolittle, W. F., Sapienza, C. (1980) Selfish genes, the phenotype paradigm and genome evolution. Nature 284: 601–603.PubMedGoogle Scholar
  41. Dover, G. (2000) How genomic and developmental dynamics affect evolutionary processes. Bioessays 22: 1153–1159.PubMedGoogle Scholar
  42. Duboule, D., Wilkins, A. S. (1998) The evolution of bricolage. Trends Genet. 14: 54–59.PubMedGoogle Scholar
  43. Eickbush, T. (1999) Exon shuffling in retrospect. Science 283: 1465–1466.PubMedGoogle Scholar
  44. Eigen, M., Gardiner, W., Schuster, P., Winkler-Oswatitsch, R. (1981) The origin of genetic information. Sci. Am. 244 (4): 88–118.PubMedGoogle Scholar
  45. Eldredge, N. (1985) Unfinished synthesis. Oxford Univ. Press, New York.Google Scholar
  46. Falconer, D. S. (1960) Introduction to quantitative genetics. Oliver and Boyd, London.Google Scholar
  47. Fenster, C. B., Galloway, L. F., Chao, L. (1997) Epistasis and its consequences for the evolution of natural populations. Trends Ecol. Evolut. 12: 282–286.Google Scholar
  48. Fontana, W., Buss, L. (1994 a) “The arrival of the fittest”: toward a theory of biological organization. Bull. Math. Biol. 56: 1–64.Google Scholar
  49. Fontana, W., Buss, L. W. (1994 b) What would be conserved if “the tape were played twice”? Proc. Natl. Acad. Sci. USA 91: 757–761.PubMedGoogle Scholar
  50. Fontana, W., Schuster, P. (1998) Continuity in evolution: On the nature of transitions. Science 280: 1451–1455.PubMedGoogle Scholar
  51. Fontana, W., Wagner, G., Buss, L. W. (1995) Beyond digital naturalism. In: Langton, C. G. (ed) Artificial life. MIT Press, Cambridge.Google Scholar
  52. Force, A., Lynch, M., Pickett, F. B., Amores, A., Yan, Y.-L., Postlethwait, J. (1999) Preservation of duplicate genes by complementary degenerative mutations. Genetics 151: 1531–1545.PubMedGoogle Scholar
  53. Forrest, S., Mitchell, M. (1993) Towards a stronger building-block hypothesis: effects of relative building-block fitness on GA performance. In: Whitley, L. D. (ed) Foundations of Genetic Algorithms. Morgon Kaufman, Palo Alto, pp. 109–126.Google Scholar
  54. Freeman, M. (2000) Feedback control of intercellular signalling in development. Nature 408: 313–319.PubMedGoogle Scholar
  55. Futuyma, D. J. (1986) Evolutionary biology. Sinauer, Sunderland.Google Scholar
  56. García-Bellido, A. (1996) Symmetries throughout organic evolution. Proc. Natl. Acad. Sci. USA 93: 14229–14232.PubMedGoogle Scholar
  57. Gellon, G., McGinnis, W. (1998) Shaping animal body plans in development and evolution by modulation of Hox expression patterns. Bioessays 20: 116–125.PubMedGoogle Scholar
  58. Gerhart, J., Kirschner, J. (1997) Cells, embryos, and evolution. Blackwell Science, Malden.Google Scholar
  59. Gibson, G., Wagner, G. (2000) Canalization in evolutionary genetics: a stabilizing theory? Bioessays 22: 372–380.PubMedGoogle Scholar
  60. Gilbert, S. F. (1998) Conceptual breakthroughs in developmental biology. J. Biosci. 23: 169–176.Google Scholar
  61. Gilbert, S. F. (2000) Developmental biology. Sinauer, Sunderland.Google Scholar
  62. Gilbert, S. F., Opitz, J. M., Raff, R. A. (1996) Resynthesizing evolutionary and developmental biology. Dev. Biol. 173: 357–372.PubMedGoogle Scholar
  63. Gilbert, W. (1978) Why genes in pieces? Nature 271: 501.PubMedGoogle Scholar
  64. Goldberg, D. E. (1989) Genetic algorithms in search, optimization, and machine learning. Addison-Wesley, Reading.Google Scholar
  65. Goodnight, C. J. (1988) Epistasis and the effect of founder events on the additive genetic variance. Evolution 42: 441–454.Google Scholar
  66. Goodnight, C. J. (1990 a) Experimental studies of community evolution. I. The response to selection at the community level. Evolution 44: 1614–1624.Google Scholar
  67. Goodnight, C. J. (1990 b) Experimental studies of community evolution. II. The ecological basis of the response to community selection. Evolution 44: 1614–1624.Google Scholar
  68. Goodnight, C. J., Schwartz, J. M., Stevens, L. (1992) Contextual analysis of group selection, soft selection, hard selection, and the evolution of altruism. Am. Nat. 140: 743–761.Google Scholar
  69. Gould, S. J. (1982) Darwinism and the expansion of the evolutionary theory. Science 216: 380–387.PubMedGoogle Scholar
  70. Gould, S. J., Eldredge, N. (1977) Punctuated equilibria: the tempo and mode of evolution reconsidered. Paleobiology 3: 115–151.Google Scholar
  71. Gould, S. J., Eldredge, N. (1993) Punctuated equilibrium comes of age. Nature 366: 223–227.PubMedGoogle Scholar
  72. Gould, S. J., Lewontin, R. C. (1979) The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme. Proc. R. Soc. Lond. B 205: 581–598.PubMedGoogle Scholar
  73. Gould, S. J., Vrba, E. S. (1982) Exaptation — a missing term in the science of form. Paleobiology 8: 4–15.Google Scholar
  74. Gray, R. (1992) Death of the gene: developmental systems strike back. In: Griffiths, P. (ed) Trees of life. Kluwer, Dordrecht, pp. 165–209.Google Scholar
  75. Griffiths, P. E., Gray, R. D. (1994) Developmental systems and evolutionary explanation. J. Philos. 91: 277–304.Google Scholar
  76. Guillemot, F. (1999) Vertebrate bHLH genes and the determination of neuronal fates. Exp. Cell Res. 253: 357–364.PubMedGoogle Scholar
  77. Hall, B. K. (1992) Evolutionary developmental biology. Chapman and Hall, London.Google Scholar
  78. Hammerschmidt, M., Brook, A., Mc Mahon, A. P. (1997) The world according to hedgehog. Trends Genet. 13: 14–21.PubMedGoogle Scholar
  79. Harper, J. L., Rosen, B. R., White, J. (1986) The growth and form of modular organisms — Preface. Phil. Trans. R. Soc. Lond. B 313: 3–5.Google Scholar
  80. Hartwell, L. H., Hopfield, J. J., Leibler, S., Murray, A. W. (1999) From molecular to modular cell biology. Nature 402 Suppl.: C 47-C 52.Google Scholar
  81. Hedrick, P., Jan, S., Holden, L. (1978) Multilocus systems in evolution. Evol. Biol. 11: 101–184.Google Scholar
  82. Heisler, I. L., Damuth, J. D. (1987) A method for analyzing selection in hierarchically structured populations. Am. Nat. 130: 582–602.Google Scholar
  83. Hertz, J., Krogh, A., Palmer, R. G. (1991) Introduction to the theory of neural computation. Addison-Wesley, Redwood City.Google Scholar
  84. Holland, J. H. (1975) Adaptation in natural and artificial systems. University of Michigan Press, Ann Arbor.Google Scholar
  85. Hull, D. L. (1980) Individuality and selection. Annu. Rev. Ecol. Syst. 11: 311–332.Google Scholar
  86. Hull, D. L. (1981) Units of evolution: a metaphysical essay. In: Jensen, U. J., Harré, R. (eds) The philosophy of evolution. The Harvester press, Brighton, pp. 23–44.Google Scholar
  87. Hurst, L. D. (1999) The evolution of genomic anatomy. Trends Ecol. Evol. 14: 108–112.PubMedGoogle Scholar
  88. Huynen, M. A., Stadler, P. F., Fontana, W. (1996) Smoothness within ruggedness: the role of neutrality in adaptation. Proc. Natl. Acad. Sci. USA 93: 397–401.PubMedGoogle Scholar
  89. Jacob, F. (1977) Evolution and tinkering. Science 196: 1161–1166.PubMedGoogle Scholar
  90. Katz, M. J. (1987) Is evolution random? In: Raff, R. A., Raff, E. C. (eds) Development as an evolutionary process. Liss, New York, pp. 285–315.Google Scholar
  91. Kauffman, S. A. (1993) The origins of order. Oxford Univ. Press, New York.Google Scholar
  92. Kauffman, S. A. (1995) At home in the universe. Oxford University Press, New York.Google Scholar
  93. Keys, D. N., Lewis, D. L., Selegue, J. E., Pearson, B. J., Goodrich, L. V., Johnson, R. L., Gates, J., Scott, M. P., Carroll, S. B. (1999) Recruitment of a hedgehog regulatory circuit in butterfly eyespot evolution. Science 283: 532–534.PubMedGoogle Scholar
  94. Kimble, J., Simpson, P. (1997) The lin-12/notch signaling pathway and its regulation. Annu. Rev. Cell Dev. Biol. 13: 333–361.PubMedGoogle Scholar
  95. Kirchhamer, C. V., Yuh, C.-H., Davidson, E. H. (1996) Modular cis-regulatory organization of developmentally expressed genes: two genes transcribed territorially in the sea urchin embryo, and additional examples. Proc. Natl. Acad. Sci. USA 93: 9322–9328.PubMedGoogle Scholar
  96. Kirschner, M., Gerhart, J. (1998) Evolvability. Proc. Natl. Acad. Sci. USA 95: 8420–8427.PubMedGoogle Scholar
  97. Krakauer, D. C., Nowak, M. A. (1999) Evolutionary preservation of redundant duplicated genes. Semin. Cell Dev. Biol. 10: 555–559.PubMedGoogle Scholar
  98. Lande, R., Arnold, S. J. (1983) The measurement of selection on correlated characters. Evolution 37: 1210–1226.Google Scholar
  99. Lewin, B. (2000) Genes VII. Oxford Univ. Press, New York.Google Scholar
  100. Lewontin, R. C. (1962) Interdeme selection controlling a polymorphism in the house mouse. Am. Nat. 96: 65–78.Google Scholar
  101. Lewontin, R. C. (1970) The units of selection. Annu. Rev. Ecol. Syst. 1: 1–18.Google Scholar
  102. Lewontin, R. C. (1974) The genetic basis of evolutionary change. Columbia Univ. Press, New York.Google Scholar
  103. Lewontin, R. C. (1978) Adaptation. Sci. Am. 239 (3): 156–169.CrossRefGoogle Scholar
  104. Lewontin, R. C. (1983) The organism as the subject and object of evolution. Scientia 118: 65–82.Google Scholar
  105. Lewontin, R. C., Kojima, K.-I. (1960) The evolutionary dynamics of complex polymorphisms. Evolution 14: 458–472.Google Scholar
  106. Lloyd, E. (1988) The structure and confirmation of evolutionary theory. Princeton Univ. Press, Princeton.Google Scholar
  107. Maconochie, M., Nonchev, S., Morrison, A., Krumlauf, R. (1996) Paralogous hox genes: function and regulation. Annu. Rev. Genet. 30: 529–556.PubMedGoogle Scholar
  108. Maturana, H. R., Varela, F. J. (1975) Autopoietic systems: A characterization of the living organization. Report 9.4 Biological Computer laboratory, University of Illinois, Urbana.Google Scholar
  109. Maynard Smith, J. (1987) How to model evolution. In: Dupré, J. (ed) The latest on the best. MIT Press, Cambridge, pp. 119–131.Google Scholar
  110. Maynard Smith, J. S. (1989) Evolutionary genetics. Oxford Univ. Press, New York.Google Scholar
  111. Maynard Smith, J. (1998) The units of selection. Novartis Foundation Symp. 213: 203–217.CrossRefGoogle Scholar
  112. Maynard Smith, J., Burian, R., Kauffman, S., Alberch, P., Campbell, J., Goodwin, B., Lande, R., Raup, D., Wolpert, L. (1985) Developmental constraints and evolution. Quart. Rev. Biol. 60: 265–287.Google Scholar
  113. Maynard Smith, J., Szathmáry, E. (1995) The major transitions in evolution. Freeman, Oxford.Google Scholar
  114. Mayr, E. (1963) Animal species and evolution. Belknap Press, Cambridge.Google Scholar
  115. McAdams, H. H., Shapiro, L. (1995) Circuit simulation of genetic networks. Science 269: 650–656.PubMedGoogle Scholar
  116. Mendoza, L., Thieffry, D., Alvarez-Buylla, E. R. (1999) Genetic control pf flower morphogenesis in Arabidopsis thaliana: a logical analysis. Bioinformatics 15: 593–606.PubMedGoogle Scholar
  117. Mezey, J. G., Cheverud, J. M., Wagner, G. P. (2000). Is the genotype-phenotype map modular?: A statistical approach using mouse quantitative trait loci data. Genetics 156: 305–311.PubMedGoogle Scholar
  118. Michod, R. E. (1997) Evolution of the individual. Amer. Nat. 150: S5-S21.Google Scholar
  119. Michod, R. E. (1999) Darwinian dynamics. Princeton Univ. Press, Princeton.Google Scholar
  120. Mjolsness, E., Sharp, D. H., Reinitz, J. (1991) A Connectionist Model of Development. J. Theor. Biol 152: 429–453.PubMedGoogle Scholar
  121. Niehrs, C., Pollet, N. (1999) Synexpression groups in eukaryotes. Nature 402: 483–487.PubMedGoogle Scholar
  122. Nowak, M. A., Boerlijst, M. C., Cooke, J., Smith, J. M. (1997) Evolution of genetic redundancy. Nature 388: 167–171.PubMedGoogle Scholar
  123. Ohno, S. (1970) Evolution by gene duplication. Springer, New York.Google Scholar
  124. Ohta, T. (1987) Simulating evolution by gene duplication. Genetics 115: 207–213.PubMedGoogle Scholar
  125. Orgel, L. E., Crick, F. H. C. (1980) Selfish DNA: the ultimate parasite. Nature 284: 604–607.PubMedGoogle Scholar
  126. Oyama, S. (1985) The ontogeny of information. Cambridge Univ. Press, Cambridge.Google Scholar
  127. Patel, N. H. (1994) Developmental evolution: Insights from studies of insect segmentation. Science 266: 581–590.PubMedGoogle Scholar
  128. Patel, N. H., Ball, E. E., Goodman, C. S. (1992) Changing role of even-skipped during the evolution of insect pattern formation. Nature 357: 339–342.PubMedGoogle Scholar
  129. Patthy, L. (1999) Genome evolution and the evolution of exon-shuffling — a review. Gene 238: 103–114.PubMedGoogle Scholar
  130. Price, G. R. (1972) Extension of covariance selection mathematics. Ann. Human Genetics 35: 485–490.CrossRefGoogle Scholar
  131. Purugganan, M. D. (1998) The molecular evolution of development. Bioessays 20: 700–711.PubMedGoogle Scholar
  132. Raff, R. A. (1996) The shape of life. Univ. of Chicago Press, Chicago.Google Scholar
  133. Rechenberg, I. (1973) Evolutionsstrategie. Frommann-Holzboog, Stuttgart.Google Scholar
  134. Reggia, J. A., Armentrout, S. L., Chou, H.-H., Peng, Y. (1993) Simple systems that exhibit self-directed replication. Science 259: 1282–1287.PubMedGoogle Scholar
  135. Reichardt, L. F., Fariñas, I. (1997) Neurotrophic factors and their receptors. In: Cowan, W. M., Jessell, T. M., Zipursky, S. L. (eds) Molecular and cellular approaches to neural development. Oxford Univ. Press, New York, pp. 220–263.Google Scholar
  136. Resnik, D. (1996) Developmental constraints and patterns: Some pertinent distinctions. J. Theor. Biol. 173: 231–240.Google Scholar
  137. Ridley, M. (1993) Evolution. Blackwell, Cambridge.Google Scholar
  138. Riedl, R. (1975) Die Ordnung des Lebendigen. Parey, Hamburg.Google Scholar
  139. Roth, G., Wake, D. B. (1989) Conservatism and innovation in the evolution of feeding in vertebrates. In: Wake, D. B., Roth, G. (eds) Complex organismal functions: Integration and evolution in vertebrates. Wiley, Chichester, pp. 7–21.Google Scholar
  140. Roth, L. (1991) Homology and hierarchies: problems solved and unresolved. J. Evol. Biol. 4: 167–194.Google Scholar
  141. Rutherford, S. L. (2000) From genotype to phenotype: buffering mechanisms and the storage of genetic information. Bioessays 22: 1095–1105.PubMedGoogle Scholar
  142. Sasai, Y., De Robertis, E. M. (1997) Ectodermal patterning in vertebrate embryos. Dev. Biol. 182: 5–20.PubMedGoogle Scholar
  143. Schank, J. C., Wimsatt, W. C. (1986) Generative entrenchment and evolution. PSA 1986 2: 33–60.Google Scholar
  144. Schank, J. C., Wimsatt, W. C. (2001) Evolvability: adaptation and modularity. In: Singh, R. S., Krimbas, C. B., Paul, D., Beatty, J. (eds) Thinking about evolution. Cambridge Univ. Press, Cambridge, pp 322–335.Google Scholar
  145. Schlosser, G. (1993) Einheit der Welt und Einheitswissenschaft. Grundlegung einer Allgemeinen Systemtheorie. Vieweg, Braunschweig.Google Scholar
  146. Schlosser, G. (1996) Der Organismus — eine Fiktion? In: Rheinberger, H. J., Weingarten, M. (eds) Jahrbuch für Geschichte und Theorie der Biologie III. Verlag für Wissenschaft und Bildung, Berlin, pp. 75–92.Google Scholar
  147. Schlosser, G. (1998) Self-re-production and functionality. A systems-theoretical approach to teleological explanation. Synthese 116: 303–354.Google Scholar
  148. Schlosser, G. (in press a) Modules — Developmental units as units of evolution? In: Schlosser,G., Wagner, G. P. (eds): Modularity in development and evolution. University of Chicago Press, Chicago.Google Scholar
  149. Schlosser, G. (in press b) Amphibian variations — the role of modules in mosaic evolution. In: Rasskin-Gutman, D., Callebaut, W. (eds) Modularity: Understanding the development and evolution of complex natural systems. MIT Press, Cambridge.Google Scholar
  150. Schlosser, G. (2001) Using heterochrony plots to detect the dissociated coevolution of characters. J. exp. Zool. (Mol. Dev. Evol.) 291: 282–304.Google Scholar
  151. Schlosser, G., Thieffry, D. (2000) Modularity in development and evolution. Bioessays 22: 1043–1045.PubMedGoogle Scholar
  152. Schwenk, K. (1994) A utilitarian approach to evolutionary constraint. Zoology 98: 251–262.Google Scholar
  153. Sharp, D. H., Reinitz, J. (1998) Prediction of mutant expression patterns using gene circuits. Biosystems 47: 79–90.PubMedGoogle Scholar
  154. Shimeld, S. M. (1999) Gene function, gene networks and the fate of duplicated genes. Semin. Cell Dev. Biol. 10: 549–553.PubMedGoogle Scholar
  155. Shubin, N., Tabin, C., Carroll, S. (1997) Fossils, genes and the evolution of animal limbs. Nature 388: 639–648.PubMedGoogle Scholar
  156. Sidow, A. (1996) Gen(om)e duplications in the evolution of early vertebrates. Curr. Opin. Genet. Develop. 6: 715–722.Google Scholar
  157. Simon, H. A. (1962) The architecture of complexity. Proc. Am. Phil. Soc. 106: 467–482.Google Scholar
  158. Simpson, P. (1997) Notch signaling in development. Perspect. Dev. Neurobiol. 4: 297–304.PubMedGoogle Scholar
  159. Smith, N. G. C., Knight, R., Hurst, L. D. (1999) Vertebrate genome evolution: a slow shuffle or a big bang? Bioessays 21: 697–703.PubMedGoogle Scholar
  160. Sober, E. (1981) Holism, individualism and the units of selection. PSA 1981: 93–121.Google Scholar
  161. Sober, E. (1984) The nature of selection. Univ. of Chicago Press, Chicago.Google Scholar
  162. Sober, E. (1987) Comments on Maynard Smith’s “How to model evolution”. In: Dupré, J. (ed) The latest on the best. MIT Press, Cambridge, pp. 133–149.Google Scholar
  163. Sober, E., Lewontin, R. C. (1982) Artifact, cause and genic selection. Philos. Science 49: 157–180.Google Scholar
  164. Sober, E., Wilson, D. S. (1994) A critical review of philosophical work on the unit of selection problem. Philos. Science 61: 534–555.Google Scholar
  165. Sober, E., Wilson, D. S. (1998) Unto others. Harvard Univ. Press, Cambridge.Google Scholar
  166. Somogyi, R., Sniegoski, C. A. (1996) Modeling the complexity of genetic networks: understanding multigenic and pleiotropic regulation. Complexity 1: 45–63.Google Scholar
  167. Štanojević, D., Hoey, T., Levine, M. (1989) Sequence-specific DNA-binding activities of the gap proteins encoded by hunchback and Krüppel in Drosophila. Nature 341: 331–335.PubMedGoogle Scholar
  168. Štanojević, D., Small, S., Levine, M. (1991) Regulation of a segmentation stripe by overlapping activators and repressors in the Drosophila embryo. Science 254: 1385–1387.PubMedGoogle Scholar
  169. Sterelny, K., Kitcher, P. (1988) The return of the gene. J. Philos. 85: 339–361.Google Scholar
  170. Striedter, G. F., Northcutt, R. G. (1991) Biological hierarchies and the concept of homology. Brain Behav Evol 38: 177–189.PubMedGoogle Scholar
  171. Stryer, L. (1981) Biochemistry. Freeman, San Francisco.Google Scholar
  172. Szathmáry, E. (1995) A classification of replicators and lambda-calculus models of biological organization. Proc. R. Soc. Lond. B 260: 279–286.Google Scholar
  173. Szathmáry, E., Maynard Smith, J. (1995) The major evolutionary transitions. Nature 374: 227–232.PubMedGoogle Scholar
  174. Szathmáry, E., Maynard Smith, J. (1997) From replicators to reproducers: the first major transitions leading to life. J. Theor. Biol. 187: 555–571.PubMedGoogle Scholar
  175. Thieffry, D., Huerta, A. M., Pérez-Rueda, E., Collado-Vides, J. (1998) From specific gene regulation to genomic networks: a global analysis of transcriptional regulation in Escherichia coli. Bioessays 20: 433–440.PubMedGoogle Scholar
  176. Thieffry, D., Romero, D. (1999) The modularity of biological regulatory networks. Biosystems 50: 49–59.PubMedGoogle Scholar
  177. Thieffry, D., Thomas, R. (1995) Dynamical behaviour of biological regulatory networks - II. Immunity control in bacteriophage lambda. Bull. Math. Biol. 57: 277–297.PubMedGoogle Scholar
  178. Thomas, R. (1978) Logical analysis of systems comprising feedback loops. J. Theor. Biol. 73: 631–656.PubMedGoogle Scholar
  179. Thomas, R. (1991) Regulatory networks seen as asynchronous automata: a logical description. J. Theor. Biol. 153: 1–23.Google Scholar
  180. Thomas, R., Thieffry, D., Kaufman, M. (1995) Dynamical behaviour of biological regulatory networks - I. Biological role of feedback loops and practical use of the concept of the loop-characteristic state. Bull. Math. Biol. 57: 247–276.PubMedGoogle Scholar
  181. Tsai, M.-J., O’Malley, B. W. (1994) Molecular mechanisms of action of steroid/thyroid receptor superfamily members. Annu. Rev. Biochem. 63: 451–486.PubMedGoogle Scholar
  182. Uexküll, J. v. (1928) Theoretische Biologie. 2nd ed. Springer, Berlin.Google Scholar
  183. Varela, F., Maturana, H. R., Uribe, R. B. (1974) Autopoiesis: The organization of living systems, its characterization and a model. Biosystems 5: 187–196.Google Scholar
  184. Von Dassow, G., Munro, E. (1999) Modularity in animal development and evolution: Elements of a conceptual framework for EvoDevo. J. Exp. Zool. (Mol. Dev. Evol.) 285: 307–325.Google Scholar
  185. Von Dassow, G., Meir, E., Munro, E. M., Odell, G. M. (2000) The segment polarity network is a robust development module. Nature 406: 188–192.Google Scholar
  186. Waddington, C. H. (1957) The strategy of the genes. George Allen and Unwin, London.Google Scholar
  187. Wade, M. J. (1985) Soft selection, hard selection, kin selection, and group selection. Am. Nat. 125: 61–73.Google Scholar
  188. Wade, M. J. (1992) Epistasis. In: Fox Keller, E., Lloyd, E. A. (eds) Keywords in evolutionary biology. Harvard University Press, Cambridge, pp. 87–91.Google Scholar
  189. Wagner, A. (1998) The fate of duplicated genes: loss or new function? Bioessays 20: 785–788.PubMedGoogle Scholar
  190. Wagner, G. P. (1981) Feedback selection and the evolution of modifiers. Acta Biotheor. 30: 79–102.PubMedGoogle Scholar
  191. Wagner, G. P. (1995) The biological role of homologues: a building block hypothesis. N. Jb. Geol. Palont. Abh. 19: 36–43.Google Scholar
  192. Wagner, G. P. (1996) Homologues, natural kinds and the evolution of modularity. Am. Zool. 36: 36–43.Google Scholar
  193. Wagner, G. P., Altenberg, L. (1996) Complex adaptations and the evolution of evolvability. Evolution 50: 967–976.Google Scholar
  194. Wagner, G. P., Bürger, R. (1985) On the evolution of dominance modifiers. II. A non-equilibrium approach to the evolution of genetic systems. J. Theor. Biol. 113: 475–500.PubMedGoogle Scholar
  195. Wagner, G. P., Booth, G., Bagheri-Chaichian, H. (1997) A population genetic theory of canalization. Evolution 51: 329–347.Google Scholar
  196. Wagner, G. P., Laubichler, M. D. (2000) Character identification in evolutionary biology: the role of the organism. Theory Biosci. 119: 20–40.Google Scholar
  197. Wagner, G. P., Laubichler, M. D., Bagheri-Chaichian, H. (1998) Genetic measurement theory of epistatic effects. Genetica 102/103: 569–580.Google Scholar
  198. Wagner, G. P., Mezey, A. (2000) Modeling the evolution of genetic architecture: A continuum of alleles model with pairwise A × A epistasis. J. Theor. Biol. 203: 163–175.PubMedGoogle Scholar
  199. Wagner, G. P., Schwenk, K. (2000) Evolutionarily stable configurations: functional integration and the evolution of phenotype stability. Evol. Biol. 31: 155–217.Google Scholar
  200. Wake, D. B., Larson, A. (1997) Multidimensional analysis of an evolving lineage. Science 238: 42–48.Google Scholar
  201. Warren, R. W., Nagy, L., Selegue, J., Gates, J., Carroll, S. (1996) Evolution of homeotic gene regulation and function in flies and butterflies. Nature 372: 458–461.Google Scholar
  202. Waters, K. (1991) Tempered realism about the force of selection. Philos. Science 58: 553–573.Google Scholar
  203. Waxman, D., Peck, J. R. (1998) Pleiotropy and the preservation of perfection. Science 279: 1210–1213.Google Scholar
  204. Webster, G., Goodwin, B. (1996) Form and transformation. Cambridge University Press, Cambridge.Google Scholar
  205. Weintraub, H. (1993) The MyoD family and myogenesis: Redundancy, networks and thresholds. Cell 75: 1241–1244.PubMedGoogle Scholar
  206. Whitlock, M. C., Phillips, P. C., Moore, F. B.-G., Tonsor, S. J. (1995) Multiple fitness peaks and epistasis. Annu. Rev. Ecol. Syst. 26: 601–629.Google Scholar
  207. Whyte, L. L. (1965) Internal factors in evolution. Tavistock Publications, London.Google Scholar
  208. Wilkins, A. S. (1997) Canalization: a molecular genetic perspective. Bioessays 19: 257–262.PubMedGoogle Scholar
  209. Wilkins, A. S. (1998) Evolutionary developmental biology: where is it going? Bioessays 20: 783–784.Google Scholar
  210. Williams, G. C. (1966) Adaptation and natural selection. Princeton Univ. Press, Princeton.Google Scholar
  211. Wilson, D. S. (1983) The group selection controversy: history and current status. Annu. Rev. Ecol. Syst. 14: 159–187.Google Scholar
  212. Wimsatt, W. C. (1980) Reductionistic research strategies and their biases in the unit of selection controversy. In: Nickles, T. (ed) Scientific discovery: case studies. Reidel, Dordrecht, pp. 213–259.Google Scholar
  213. Wimsatt, W. C. (1981) Units of selection and the structure of the multilevel genome. PSA 1980 2: 122–183.Google Scholar
  214. Wimsatt, W. C. (1986) Developmental constraints, generative entrenchment, and the innate-acquired distinction. In: Bechtel, W. (ed). Integrating scientific disciplines. Nijhoff Publ. Dordrecht, pp. 185–208.Google Scholar
  215. Wray, G. A. (1994) Developmental evolution - new paradigms and paradoxes. Dev. Genet. 15: 1–6.PubMedGoogle Scholar
  216. Wright, S. (1931) Evolution in Mendelian populations. Genetics 16: 97–159.PubMedGoogle Scholar
  217. Wright, S. (1988) Surface of selective value revisited. Am. Nat. 131: 115–123.Google Scholar
  218. Xu, X. L., Weinstein, M., Li, C. L., Deng, C. X. (1999) Fibroblast growth factor receptors (FGFRs) and their roles in limb development. Cell Tissue Res. 296: 33–43.PubMedGoogle Scholar
  219. Yen, P. M., Chin, W. W. (1994) New advances in understanding the molecular mechanisms of thyroid hormone action. Trends Endocrinol. Metab. 5: 65–72.PubMedGoogle Scholar
  220. Yuh, C.-H., Bolouri, H., Davidson, E. H. (1998) Genomic cis-regulatory logic: axperimental and computaional analysis of a sea urchin gene. Science 279: 1896–1902.PubMedGoogle Scholar
  221. Zuckerkandl, E. (1994) Molecular pathways to parallel evolution. 1. Gene nexuses and their morphological correlates. J. Mol. Evol. 39: 661–678.PubMedGoogle Scholar
  222. Zuckerkandl, E. (1997) Neutral and nonneutral mutations: the creative mix - evolution of complexity in gene interaction systems. J. Mol. Evol. 44, Suppl. 1: S2-S8.PubMedGoogle Scholar

Copyright information

© Urban & Fischer Verlag 2002

Authors and Affiliations

  1. 1.Brain Research InstituteUniversity of Bremen, FB 2BremenGermany

Personalised recommendations