Review Article | Published:

The emerging conceptual framework of evolutionary developmental biology

Nature volume 415, pages 757764 (14 February 2002) | Download Citation

Subjects

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.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

References

  1. 1.

    Uber Entwicklungsgeschichte der Tiere: Beobachtung und Reflexion (Bornträger, Königsberg, 1828).

  2. 2.

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

  3. 3.

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

  4. 4.

    & 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).

  5. 5.

    , , , & A homologous protein-coding sequence in Drosophila homeotic genes and its conservation in other metazoans. Cell 37, 403–408 (1984).

  6. 6.

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

  7. 7.

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

  8. 8.

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

  9. 9.

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

  10. 10.

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

  11. 11.

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

  12. 12.

    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).

  13. 13.

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

  14. 14.

    & The Life Science: Current Ideas of Biology (Wildwood House, London, 1977).

  15. 15.

    , & Comparative development of anurans: using phylogeny to understand ontogeny. Am. Zool. 41, 538–551 (2001).

  16. 16.

    & Zebrafish in context: uses of a laboratory model in comparative studies. Dev. Biol. 210, 1–14 (1999).

  17. 17.

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

  18. 18.

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

  19. 19.

    Embryos and Ancestors (Clarendon, Oxford, 1940).

  20. 20.

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

  21. 21.

    & Mutations affecting segment number and polarity in Drosophila. Nature 287, 795–801 (1980).

  22. 22.

    & Embryos, Genes and Evolution: the Developmental Genetic Basis of Evolutionary Change (Macmillan, New York, 1983).

  23. 23.

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

  24. 24.

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

  25. 25.

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

  26. 26.

    & Radical alterations in the roles of homeobox genes during echinoderm evolution. Nature 389, 718–721 (1997).

  27. 27.

    Considérations générales sur la vertèbre. Mem. Mus. Hist. Nat. 9, 89–119 (1822).

  28. 28.

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

  29. 29.

    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).

  30. 30.

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

  31. 31.

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

  32. 32.

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

  33. 33.

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

  34. 34.

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

  35. 35.

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

  36. 36.

    & Phenotypic Evolution: a Reaction Norm Perspective (Sinauer, Sunderland, 1998).

  37. 37.

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

  38. 38.

    & Heterochrony: the Evolution of Ontogeny (Plenum, New York, 1991).

  39. 39.

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

  40. 40.

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

  41. 41.

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

  42. 42.

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

  43. 43.

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

  44. 44.

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

  45. 45.

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

  46. 46.

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

  47. 47.

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

  48. 48.

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

  49. 49.

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

  50. 50.

    Ecological Genetics 3rd edn (Chapman & Hall, London, 1971)

  51. 51.

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

  52. 52.

    & Homoplasy and developmental constraint: a model and an example from plants. Am. Zool. 40, 759–769 (2000).

  53. 53.

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

  54. 54.

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

  55. 55.

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

  56. 56.

    , & Out on a limb: parallels in vertebrate and invertebrate limb patterning and the origin of appendages. Am. Zool. 39, 650–663 (1999).

  57. 57.

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

  58. 58.

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

  59. 59.

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

  60. 60.

    The ancestry of segmentation. Nature 387, 25–26 (1997).

  61. 61.

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

  62. 62.

    , , & 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).

  63. 63.

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

  64. 64.

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

  65. 65.

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

  66. 66.

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

  67. 67.

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

  68. 68.

    & 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).

  69. 69.

    , & Variation and selection at the CAULIFLOWER floral homeotic gene accompanying the evolution of domesticated Brassica oleracea. Genetics 155, 855–862 (2000).

  70. 70.

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

  71. 71.

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

  72. 72.

    & 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).

  73. 73.

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

  74. 74.

    , & The zootype and the phylotypic stage. Nature 361, 490–492 (1993).

  75. 75.

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

  76. 76.

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

  77. 77.

    & Homology evolving. Trends Ecol. Evol. 16, 434–440 (2001).

  78. 78.

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

  79. 79.

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

  80. 80.

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

  81. 81.

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

  82. 82.

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

  83. 83.

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

  84. 84.

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

  85. 85.

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

  86. 86.

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

  87. 87.

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

  88. 88.

    , , & Transcriptional regulation of cytoskeletal functions and segmentation by a novel maternal pair-rule gene, lilliputian. Development 128, 801–813 (2001).

  89. 89.

    , , & The segment polarity network is a robust developmental module. Nature 406, 188–192 (2000).

  90. 90.

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

  91. 91.

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

  92. 92.

    , & The anterior determinant bicoid of Drosophila is a derived Hox class 3 gene. Proc. Natl Acad. Sci. USA 96, 3786–3789 (1999).

  93. 93.

    , , , & Divergent structure and function of the bicoid gene in Muscoidea fly species. Evol. Dev. 3, 251–262 (2001).

  94. 94.

    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).

  95. 95.

    , , , & Dax, a locust Hox gene related to fushi-tarazu but showing no pair-rule expression. Development 120, 1561–1572 (1994).

  96. 96.

    , & Pax group III genes and the evolution of insect pair-rule patterning. Am. Zool. 40, 992 (2000).

  97. 97.

    , & 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).

  98. 98.

    , & Phenotypic and dynamical transitions in model genetic networks I. Emergency of patterns and genotype-phenotype relationships. Evol. Dev. 3, 84–94 (2001).

  99. 99.

    , & Phenotypic and dynamical transitions in model genetic networks II. Application to the evolution of segmentation mechanisms. Evol. Dev. 3, 95–103 (2001).

Download references

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.

Author information

Affiliations

  1. Ecology Centre, School of Sciences, University of Sunderland, Sunderland SR1 3SD, UK

    • Wallace Arthur

Authors

  1. Search for Wallace Arthur in:

Corresponding author

Correspondence to Wallace Arthur.

About this article

Publication history

Published

DOI

https://doi.org/10.1038/415757a

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.