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The emerging conceptual framework of evolutionary developmental biology

Abstract

Over the last twenty years, there has been rapid growth of a new approach to understanding the evolution of organismic form. This evolutionary developmental biology, or ‘evo-devo’, is focused on the developmental genetic machinery that lies behind embryological phenotypes, which were all that could be studied in the past. Are there any general concepts emerging from this new approach, and if so, how do they impact on the conceptual structure of traditional evolutionary biology? In providing answers to these questions, this review assesses whether evo-devo is merely filling in some missing details, or whether it will cause a large-scale change in our thinking about the evolutionary process.

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Figure 1: The recapitulatory aspect of the evolution of development in lineages that exhibit increasing phenotypic complexity.
Figure 2: Conservation and change in a developmental mechanism.

References

  1. 1

    Von Baer, K. E. Uber Entwicklungsgeschichte der Tiere: Beobachtung und Reflexion (Bornträger, Königsberg, 1828).

    Book  Google Scholar 

  2. 2

    Haeckel, E. Generelle Morphologie der Organismen (Georg Reimer, Berlin, 1866).

    Book  Google Scholar 

  3. 3

    Haeckel, E. The Evolution of Man: a Popular Exposition of the Principal Points of Human Ontogeny and Phylogeny (Appleton, New York, 1896).

    Book  Google Scholar 

  4. 4

    Scott, M. P. & Weiner, A. J. Structural relationships among genes that control development: sequence homology between the Antennapedia, Ultrabithorax and fushi tarazu loci of Drosophila. Proc. Natl Acad. Sci. USA 81, 4115–4119 (1984).

    ADS  CAS  PubMed  Article  Google Scholar 

  5. 5

    McGinnis, W., Garber, R. L., Wirz, J., Kuroiwa, A. & Gehring, W. J. A homologous protein-coding sequence in Drosophila homeotic genes and its conservation in other metazoans. Cell 37, 403–408 (1984).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  6. 6

    Averof, M. & Akam, M. Hox genes and the diversification of insect and crustacean body plans. Nature 376, 420–423 (1995).

    ADS  CAS  PubMed  Article  Google Scholar 

  7. 7

    Wray, G. A. & Bely, A. E. in The Evolution of Developmental Mechanisms (eds Akam, M., Holland, P., Ingham, P. & Wray, G.). Development (Suppl.) (Company of Biologists, Cambridge, 1994).

    Google Scholar 

  8. 8

    Gould, S. J. Ontogeny and Phylogeny (Harvard Univ. Press, Cambridge, Massachusetts, 1977).

    Google Scholar 

  9. 9

    Arthur, W. The Origin of Animal Body Plans: a Study in Evolutionary Developmental Biology (Cambridge Univ. Press, Cambridge, 1997).

    Book  Google Scholar 

  10. 10

    Sander, K. in Development and Evolution (eds Goodwin, B. C., Holder, N. & Wylie, C. C.) 137–159 (Cambridge Univ. Press, Cambridge, 1983).

    Google Scholar 

  11. 11

    Duboule, D. in The Evolution of Developmental Mechanisms (eds Akam, M., Holland, P., Ingham, P. & Wray, G.) Development (Suppl.) (Company of Biologists, Cambridge, 1994).

    Google Scholar 

  12. 12

    Richardson, M. K. et al. There is no highly conserved embryonic stage in the vertebrates: implications for current theories of evolution and development. Anat. Embryol. 196, 91–106 (1997).

    CAS  PubMed  Article  Google Scholar 

  13. 13

    Hennig, W. Phylogenetic Systematics (Univ. Illinois Press, Urbana, 1966).

    Google Scholar 

  14. 14

    Medawar, P. B. & Medawar, J. S. The Life Science: Current Ideas of Biology (Wildwood House, London, 1977).

    Google Scholar 

  15. 15

    Maglia, A. M., Pugener, L. A. & Trueb, L. Comparative development of anurans: using phylogeny to understand ontogeny. Am. Zool. 41, 538–551 (2001).

    Google Scholar 

  16. 16

    Metscher, B. D. & Ahlberg, P. E. Zebrafish in context: uses of a laboratory model in comparative studies. Dev. Biol. 210, 1–14 (1999).

    CAS  PubMed  Article  Google Scholar 

  17. 17

    Nelson, G. J. Ontogeny, phylogeny, paleontology and the biogenetic law. Syst. Zool. 27, 324–345 (1978).

    Article  Google Scholar 

  18. 18

    Roux, W. The problems, methods and scope of developmental mechanics. Biol. Lect. Mar. Biol. Lab., Woods Hole 149–190 (Ginn, Boston, 1894).

  19. 19

    De Beer, G. R. Embryos and Ancestors (Clarendon, Oxford, 1940).

    Google Scholar 

  20. 20

    Waddington, C. H. The Strategy of the Genes (Allen & Unwin, London, 1957).

    Google Scholar 

  21. 21

    Nüsslein-Volhard, C. & Wieschaus, E. Mutations affecting segment number and polarity in Drosophila. Nature 287, 795–801 (1980).

    ADS  PubMed  Article  Google Scholar 

  22. 22

    Raff, R. A. & Kaufman, T. C. Embryos, Genes and Evolution: the Developmental Genetic Basis of Evolutionary Change (Macmillan, New York, 1983).

    Google Scholar 

  23. 23

    Arthur, W. Mechanisms of Morphological Evolution: a Combined Genetic, Developmental and Ecological Approach (Wiley, Chichester, 1984).

    Google Scholar 

  24. 24

    Patel, N. H. Developmental evolution: insights from studies of insect segmentation. Science 266, 581–590 (1994).

    ADS  CAS  PubMed  Article  Google Scholar 

  25. 25

    Patel, N. H. in The Evolution of Developmental Mechanisms (eds Akam, M., Holland, P., Ingham, P. & Wray, G.) Development (Suppl.) (Company of Biologists, Cambridge, 1994).

    Google Scholar 

  26. 26

    Lowe, C. J. & Wray, G. A. Radical alterations in the roles of homeobox genes during echinoderm evolution. Nature 389, 718–721 (1997).

    ADS  CAS  PubMed  Article  Google Scholar 

  27. 27

    Geoffroy Saint-Hilaire, E. Considérations générales sur la vertèbre. Mem. Mus. Hist. Nat. 9, 89–119 (1822).

    Google Scholar 

  28. 28

    Holley, S. A. et al. A conserved system for dorsal-ventral patterning in insects and vertebrates involving sog and chordin. Nature 376, 249–253 (1995).

    ADS  CAS  PubMed  Article  Google Scholar 

  29. 29

    Darwin, C. On the Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life (John Murray, London, 1859).

    Book  Google Scholar 

  30. 30

    Dobzhansky, T. Genetics and the Origin of Species (Columbia Univ. Press, New York, 1937).

    Google Scholar 

  31. 31

    Mayr, E. Systematics and the Origin of Species (Columbia Univ. Press, New York, 1942).

    Google Scholar 

  32. 32

    Simpson, G. G. Tempo and Mode in Evolution (Columbia Univ. Press, New York, 1944).

    Google Scholar 

  33. 33

    Arthur, W. The concept of developmental reprogramming and the quest for an inclusive theory of evolutionary mechanisms. Evol. Dev. 2, 49–57 (2000).

    CAS  PubMed  Article  Google Scholar 

  34. 34

    Robert, J. S. Interpreting the homeobox: metaphors of gene action and activation in development and evolution. Evol. Dev. 3, 287–295 (2001).

    CAS  PubMed  Article  Google Scholar 

  35. 35

    Davidson, E. H. Gene Activity in Early Development 3rd edn (Academic, Orlando, 1986).

    Google Scholar 

  36. 36

    Schlichting, C. D. & Pigliucci, M. Phenotypic Evolution: a Reaction Norm Perspective (Sinauer, Sunderland, 1998).

    Google Scholar 

  37. 37

    Wells, C. L. & Pigliucci, M. Adaptive phenotypic plasticity: the case of heterophylly in aquatic plants. Persp. Plant Ecol. Evol. Syst. 3, 1–18 (2000).

    Article  Google Scholar 

  38. 38

    McKinney, M. L. & McNamara, K. J. Heterochrony: the Evolution of Ontogeny (Plenum, New York, 1991).

    Book  Google Scholar 

  39. 39

    Hall, B. K. Evolutionary Developmental Biology 2nd edn (Kluwer, Dordrecht, 1999).

    Book  Google Scholar 

  40. 40

    Zelditch, M. L. & Fink, W. L. Heterochrony and heterotopy: stability and innovation in the evolution of form. Paleobiology 22, 241–254 (1996).

    Article  Google Scholar 

  41. 41

    Yampolsky, L. Y. & Stoltzfus, A. Mutation bias as an orienting factor in selective evolution. Evol. Dev. 3, 73–83 (2001).

    CAS  PubMed  Article  Google Scholar 

  42. 42

    Raff, R. A. Evo-devo: the evolution of a new discipline. Nature Rev. Genet. 1, 74–79 (2000).

    CAS  PubMed  Article  Google Scholar 

  43. 43

    Maynard Smith, J. et al. Developmental constraints and evolution. Q. Rev. Biol. 60, 265–287 (1985).

    Article  Google Scholar 

  44. 44

    Gould, S. J. & Lewontin, R. C. The Spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme. Proc. R. Soc. Lond. B 205, 581–598 (1979).

    ADS  CAS  PubMed  Article  Google Scholar 

  45. 45

    Arthur, W. Developmental drive: an important determinant of the direction of phenotypic evolution. Evol. Dev. 3, 271–278 (2001).

    CAS  PubMed  Article  Google Scholar 

  46. 46

    Geliva, E. A. Meiotic drive in the sex chromosome system of the varying lemming, Dicrostomyx torquatus Pall. (Rodentia: Microtinae). Heredity 59, 383–389 (1987).

    Article  Google Scholar 

  47. 47

    Dover, G. A. Molecular drive: a cohesive mode of species evolution. Nature 299, 111–117 (1982).

    ADS  CAS  PubMed  Article  Google Scholar 

  48. 48

    Mallet, J. Hybrid zones of Heliconius butterflies in Panama and the stability and movement of warning colour clines. Heredity 56, 191–202 (1986).

    Article  Google Scholar 

  49. 49

    Fisher, R. A. The Genetical Theory of Natural Selection (Clarendon, Oxford, 1930).

    MATH  Book  Google Scholar 

  50. 50

    Ford, E. B. Ecological Genetics 3rd edn (Chapman & Hall, London, 1971)

    Google Scholar 

  51. 51

    Goodwin, B. How the Leopard Changed its Spots: The Evolution of Complexity (Weidenfeld & Nicolson, London, 1994).

    Google Scholar 

  52. 52

    Donoghue, M. J. & Ree, R. H. Homoplasy and developmental constraint: a model and an example from plants. Am. Zool. 40, 759–769 (2000).

    Google Scholar 

  53. 53

    Arthur, W. & Farrow, M. The pattern of variation in centipede segment number as an example of developmental constraint in evolution. J. Theor. Biol. 200, 183–191 (1999).

    CAS  PubMed  Article  Google Scholar 

  54. 54

    Gould, S. J. & Vrba, E. S. Exaptation—a missing term in the science of form. Paleobiology 8, 4–15 (1982).

    Article  Google Scholar 

  55. 55

    Chipman, A. D. Developmental exaptation and evolutionary change. Evol. Dev. 3, 299–301 (2001).

    CAS  PubMed  Article  Google Scholar 

  56. 56

    Tabin, C. J., Carroll, S. B. & Panganiban, G. Out on a limb: parallels in vertebrate and invertebrate limb patterning and the origin of appendages. Am. Zool. 39, 650–663 (1999).

    CAS  Article  Google Scholar 

  57. 57

    Minelli, A. Limbs and tail as evolutionarily diverging duplicates of the main body axis. Evol. Dev. 2, 157–165 (2000).

    CAS  PubMed  Article  Google Scholar 

  58. 58

    Abouheif, E. et al. Homology and developmental genes. Trends Genet. 13, 432–433 (1997).

    CAS  PubMed  Article  Google Scholar 

  59. 59

    Clark, R. B. Dynamics in Metazoan Evolution: the Origin of the Coelom and Segments (Clarendon, Oxford, 1964).

    Google Scholar 

  60. 60

    De Robertis, E. M. The ancestry of segmentation. Nature 387, 25–26 (1997).

    ADS  PubMed  Google Scholar 

  61. 61

    Aguinaldo, A. M. A. et al. Evidence for a clade of nematodes, arthropods and other moulting animals. Nature 387, 489–493 (1997).

    CAS  PubMed  Article  Google Scholar 

  62. 62

    Holland, L. Z., Kene, M., Williams, N. A. & Holland, N. D. Sequence and embryonic expression of the amphioxus engrailed gene (AmphiEn): the metameric pattern of transcription resembles that of its segment-polarity homolog in Drosophila. Development 124, 1723–1732 (1997).

    CAS  PubMed  Google Scholar 

  63. 63

    Panganiban, G. et al. The origin and evolution of animal appendages. Proc. Natl Acad. Sci. USA 94, 5162–5166 (1997).

    ADS  CAS  PubMed  Article  Google Scholar 

  64. 64

    Gibson, G. & Hogness, D. S. Effect of polymorphism in the Drosophila regulatory gene Ultrabithorax on homeotic stability. Science 271, 200–203 (1996).

    ADS  CAS  PubMed  Article  Google Scholar 

  65. 65

    Stern, D. L. A role of Ultrabithorax in morphological differences between Drosophila species. Nature 396, 463–466 (1998).

    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

  66. 66

    Kettle, C. & Arthur, W. Latitudinal cline in segment number in an arthropod species, Strigamia maritima. Proc. R. Soc. Lond. B 267, 1393–1397 (2000).

    CAS  Article  Google Scholar 

  67. 67

    Ng, M. & Yanofsky, M. F. Function and evolution of the plant MADS-box gene family. Nature Rev. Genet. 2, 186–193 (2001).

    CAS  PubMed  Article  Google Scholar 

  68. 68

    Purugganan, M. D. & Suddith, J. I. Molecular population genetics of the Arabidopsis CAULIFLOWER regulatory gene: Nonneutral evolution and naturally occurring variation in floral homeotic function. Proc. Natl Acad. Sci. USA 95, 8130–8134 (1998).

    ADS  CAS  PubMed  Article  Google Scholar 

  69. 69

    Purugganan, M. D., Boyles, A. L. & Suddith, J. I. Variation and selection at the CAULIFLOWER floral homeotic gene accompanying the evolution of domesticated Brassica oleracea. Genetics 155, 855–862 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  70. 70

    Turner, J. R. G. Butterfly mimicry: the genetical evolution of an adaptation. Evol. Biol. 10, 163–226 (1977).

    Google Scholar 

  71. 71

    Brakefield, P. M. et al. Development, plasticity and evolution of butterfly eyespot patterns. Nature 384, 236–242 (1996).

    ADS  CAS  PubMed  Article  Google Scholar 

  72. 72

    Roth, G. & Wake, D. B. Trends in the functional morphology and sensorimotor control of feeding behaviour in salamanders: an example of the role of internal dynamics in evolution. Acta Biotheor. 34, 175–192 (1985).

    CAS  PubMed  Article  Google Scholar 

  73. 73

    Wagner, G. P. & Schwenk, K. Evolutionarily stable configurations: functional integration and the evolution of phenotypic stability. Evol. Biol. 31, 155–217 (2000).

    Article  Google Scholar 

  74. 74

    Slack, J. M. W., Holland, P. W. H. & Graham, C. F. The zootype and the phylotypic stage. Nature 361, 490–492 (1993).

    ADS  CAS  PubMed  Article  Google Scholar 

  75. 75

    Owen, R. On the Archetype and Homologies of the Vertebrate Skeleton (John van Voorst, London, 1848).

    Book  Google Scholar 

  76. 76

    Hall, B. K. (ed.) Homology: the Hierarchical Basis of Comparative Biology (Academic, San Diego, 1994).

    Google Scholar 

  77. 77

    Mindell, D. P. & Meyer, A. Homology evolving. Trends Ecol. Evol. 16, 434–440 (2001).

    Article  Google Scholar 

  78. 78

    Raff, R. A. The Shape of Life: Genes, Development and the Evolution of Animal Form (Chicago Univ. Press, Chicago, 1996).

    Book  Google Scholar 

  79. 79

    Kirschner, M. & Gerhart, J. Evolvability. Proc. Natl Acad. Sci. USA 95, 8420–8427 (1998).

    ADS  CAS  PubMed  Article  Google Scholar 

  80. 80

    Holland, P. W. H. Gene duplication: past, present and future. Sem. Cell Dev. Biol. 10, 541–547 (1999).

    MathSciNet  CAS  Article  Google Scholar 

  81. 81

    Whyte, L. L. Internal Factors in Evolution (Tavistock, London, 1965).

    Book  Google Scholar 

  82. 82

    Wimsatt, W. C. in Integrating Scientific Disciplines (ed. Bechtel, W.) (Martinus-Nijhoff, Dordrecht, 1986).

    Google Scholar 

  83. 83

    Riedl, R. Order in Living Organisms: a Systems Analysis of Evolution (Wiley, Chichester, 1978).

    Google Scholar 

  84. 84

    Rutherford, S. L. & Lindquist, S. Hsp90 as a capacitor for morphological evolution. Nature 396, 336–342 (1998).

    ADS  CAS  PubMed  Article  Google Scholar 

  85. 85

    Salser, S. J. & Kenyon, C. A C. elegans Hox gene switches on, off, on and off again to regulate proliferation, differentiation and morphogenesis. Development 122, 1651–1661 (1996).

    CAS  PubMed  Google Scholar 

  86. 86

    Xu, P.-X. et al. Regulation of Pax6 expression is conserved between mice and flies. Development 126, 383–395 (1999).

    CAS  PubMed  Google Scholar 

  87. 87

    Ingham, P. W. The molecular genetics of embryonic pattern formation in Drosophila. Nature 335, 25–34 (1988).

    ADS  CAS  PubMed  Article  Google Scholar 

  88. 88

    Tang, A. H., Neufeld, T. P., Rubin, G. M. & Mueller, H.-A. J. Transcriptional regulation of cytoskeletal functions and segmentation by a novel maternal pair-rule gene, lilliputian. Development 128, 801–813 (2001).

    CAS  PubMed  Google Scholar 

  89. 89

    von Dassow, G., Meir, E., Munro, E. M. & Odell, G. M. The segment polarity network is a robust developmental module. Nature 406, 188–192 (2000).

    ADS  CAS  PubMed  Article  Google Scholar 

  90. 90

    Basler, K. & Struhl, G. Compartment boundaries and the control of Drosophila limb pattern by hedgehog protein. Nature 368, 208–214 (1994).

    ADS  CAS  PubMed  Article  Google Scholar 

  91. 91

    Holleman, T., Bellefroid, E. & Pieler, T. The Xenopus homologue of the Drosophila gene tailless has a function in early eye development. Development 125, 2425–2432 (1998).

    Google Scholar 

  92. 92

    Stauber, M., Jäckle, H. & Schmidt-Ott, U. The anterior determinant bicoid of Drosophila is a derived Hox class 3 gene. Proc. Natl Acad. Sci. USA 96, 3786–3789 (1999).

    ADS  CAS  PubMed  Article  Google Scholar 

  93. 93

    Shaw, P. J., Salameh, A., McGregor, A. P., Bala, S. & Dover, G. A. Divergent structure and function of the bicoid gene in Muscoidea fly species. Evol. Dev. 3, 251–262 (2001).

    CAS  PubMed  Article  Google Scholar 

  94. 94

    McGregor, A. P. et al. Rapid restructuring of bicoid-dependent hunchback promoters within and between Dipteran species: implications for molecular co-evolution. Evol. Dev. 3, 397–407 (2001).

    CAS  PubMed  Article  Google Scholar 

  95. 95

    Dawes, R., Dawson, I., Falciani, F., Tear, G. & Akam, M. Dax, a locust Hox gene related to fushi-tarazu but showing no pair-rule expression. Development 120, 1561–1572 (1994).

    CAS  PubMed  Google Scholar 

  96. 96

    Davis, G. K., Jaramillo, C. A. & Patel, N. H. Pax group III genes and the evolution of insect pair-rule patterning. Am. Zool. 40, 992 (2000).

    Google Scholar 

  97. 97

    Schroeder, R., Jay, D. G. & Tautz, D. Elimination of Eve protein by CALI in the short germ band insect Tribolium suggests a conserved pair-rule function for even-skipped. Mech. Dev. 80, 191–195 (1999).

    Article  Google Scholar 

  98. 98

    Salazar-Ciudad, I., Newman, S. A. & Solé, R. V. Phenotypic and dynamical transitions in model genetic networks I. Emergency of patterns and genotype-phenotype relationships. Evol. Dev. 3, 84–94 (2001).

    CAS  PubMed  Article  Google Scholar 

  99. 99

    Salazar-Ciudad, I., Solé, R. V. & Newman, S. A. Phenotypic and dynamical transitions in model genetic networks II. Application to the evolution of segmentation mechanisms. Evol. Dev. 3, 95–103 (2001).

    CAS  PubMed  Article  Google Scholar 

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Acknowledgements

I thank P. Ahlberg and A. Panchen for comments on the manuscript; J. Blackburn, A. Cherrill and P. Griffin for photographs; P. Giblin for production of the typescript; and the Natural Environment Research Council for financial support for my current research.

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Arthur, W. The emerging conceptual framework of evolutionary developmental biology. Nature 415, 757–764 (2002). https://doi.org/10.1038/415757a

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