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Evo–devo: extending the evolutionary synthesis

Nature Reviews Genetics volume 8, pages 943949 (2007) | Download Citation

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Abstract

Evolutionary developmental biology (evo–devo) explores the mechanistic relationships between the processes of individual development and phenotypic change during evolution. Although evo–devo is widely acknowledged to be revolutionizing our understanding of how the development of organisms has evolved, its substantial implications for the theoretical basis of evolution are often overlooked. This essay identifies major theoretical themes of current evo–devo research and highlights how its results take evolutionary theory beyond the boundaries of the Modern Synthesis.

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References

  1. 1.

    & (eds) From Embryology to Evo–Devo: A History of Developmental Evolution (MIT Press, Cambridge, 2007).

  2. 2.

    Biological Emergences: Evolution by Natural Experiment (MIT Press, Cambridge, 2007).

  3. 3.

    & Fossilized metazoan embryos from the earliest Cambrian. Science 277, 1645–1648 (1997).

  4. 4.

    & Heterochrony (Plenum, New York, 1991).

  5. 5.

    , & Fossils, genes and the evolution of animal limbs. Nature 388, 639–648 (1997).

  6. 6.

    , , , & Epigenetic interactions and the structure of phenotypic variation in the cranium. Evol. Dev. 9, 76–91 (2007).

  7. 7.

    The Geometry of Evolution (Cambridge Univ. Press, Cambridge, 2007).

  8. 8.

    The emerging conceptual framework of evolutionary developmental biology. Nature 415, 757–764 (2002).

  9. 9.

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

  10. 10.

    The Regulatory Genome: Gene Regulatory Networks in Development and Evolution (Academic, San Diego, 2006).

  11. 11.

    The Evolution of Developmental Pathways (Sinauer Associates, Sunderland, 2002).

  12. 12.

    , & From DNA to Diversity (Blackwell Science, Malden, 2005).

  13. 13.

    & A developmental analysis of an evolutionary trend: digital reduction in amphibians. Evolution 39, 8–23 (1985).

  14. 14.

    , & Homeotic duplication of the pelvic body segment in regenerating tadpole tails induced by retinoic acid. Dev. Genes Evol. 206, 344–348 (1996).

  15. 15.

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

  16. 16.

    , & (eds) Environment, Development, and Evolution (MIT Press, Cambridge, 2003).

  17. 17.

    Developmental Plasticity and Evolution (Oxford Univ. Press, Oxford, 2003).

  18. 18.

    , & Evolutionary modification of development in mammalian teeth: quantifying gene expression patterns and topography. Proc. Natl Acad. Sci. USA 97, 14444–14448 (2000).

  19. 19.

    et al. Computer based three-dimensional visualization of developmental gene expression. Nature Genet. 25, 147–152 (2000).

  20. 20.

    et al. High resolution episcopic microscopy: rapid 3D-analysis of gene expression and tissue architecture. Anat. Embryol. 211, 213–221 (2006).

  21. 21.

    et al. A field approach to three-dimensional gene expression pattern characterization. Appl. Physics Lett. 86, 143901–143903 (2005).

  22. 22.

    , , , & Comparison of cranial ontogenetic trajectories among hominoids. J. Hum. Evol. 46, 679–697 (2004).

  23. 23.

    et al. The brachymorph mouse and the developmental-genetic basis for canalization and morphological integration. Evol. Dev. 8, 61–73 (2006).

  24. 24.

    , , & Dynamical mechanisms for skeletal pattern formation in the vertebrate limb. Proc. R. Soc. Lond. B Biol. Sci. 271, 1713–1722 (2004).

  25. 25.

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

  26. 26.

    & Epigenetic mechanisms of character origination. J. Exp. Zool. B Mol. Dev. Evol. 288, 304–317 (2000).

  27. 27.

    & Rapid evolution of cis-regulatory sequences via local point mutations. Mol. Biol. Evol. 18, 1764–1770 (2001).

  28. 28.

    , , & Origin of a substantial fraction of human regulatory sequences from transposable elements. Trends Genet. 19, 68–72 (2003).

  29. 29.

    & The evolutionary demography of duplicate genes. J. Struct. Funct. Genomics 3, 35–44 (2003).

  30. 30.

    , & Variation in gene expression within and among natural populations. Nature Genet. 32, 261–266 (2002).

  31. 31.

    & Multiple regulatory changes contribute to the evolution of the Caenorhabditis lin-48 ovo gene. Genes Dev. 16, 2345–2349 (2002).

  32. 32.

    & Evolution of functionally conserved enhancers can be accelerated in large populations: a population-genetic model. Proc. Biol. Sci. 269, 953–960 (2002).

  33. 33.

    The evolution of arthropod segmentation: insights from comparisons of gene expression patterns. Dev. Suppl. 1994, 201–207 (1994).

  34. 34.

    , , & Hox genes and the evolution of vertebrate axial morphology. Development 121, 333–346 (1995).

  35. 35.

    & Homeotic genes and the arthropod head: expression patterns of the labial, proboscipedia, and Deformed genes in crustaceans and insects. Proc. Natl Acad. Sci. USA 96, 10224–10229 (1999).

  36. 36.

    & The tetrapod limb: a hypothesis on its origin. J. Exp. Zool. B Mol. Dev. Evol. 291, 226–240 (2001).

  37. 37.

    Developmental processes underlying heterochrony as an evolutionary mechanism. Can. J. Zool. 62, 1–7 (1984).

  38. 38.

    & Heterochrony: developmental mechanisms and evolutionary results. J. Evol. Biol. 2, 409–434 (1989).

  39. 39.

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

  40. 40.

    & Modularity in animal development and evolution: elements of a conceptual framework for evodevo. J. Exp. Zool. B Mol. Dev. Evol. 285, 307–325 (1999).

  41. 41.

    & (eds) Modularity in Development and Evolution (Univ. Chicago Press, Chicago, 2004).

  42. 42.

    & Modularity: Understanding the Development and Evolution of Complex Natural Systems (MIT Press, Cambridge, 2005).

  43. 43.

    & Complex adaptations and the evolution of evolvability. Evolution 50, 967–976 (1996).

  44. 44.

    in Origination of Organismal Form (eds Müller, G. B. & Newman, S. A.) 51–69 (MIT Press, Cambridge, 2003).

  45. 45.

    The developmental genetics of homology. Nature Rev. Genet. 8, 473–479 (2007).

  46. 46.

    , , & Developmental reaction norms: the interactions among allometry, ontogeny, and plasticity. Plant Species Biol. 11, 69–85 (1996).

  47. 47.

    & Seasonal polyphenism in Bicyclus (Lepidoptera: Satyridae) butterflies: different climates need different cues. Biol. J. Linn. Soc. Lond. 66, 345–356 (1999).

  48. 48.

    & (eds) The Ecology and Evolution of Inducible Defenses (Princeton Univ. Press, Princeton, 1999).

  49. 49.

    3rd, & Phenotypic plasticity of reproductive effort in a colonial ascidian, Botryllus schlosseri. J. Exp. Zoolog. Part A Comp. Exp. Biol. 297, 180–188 (2003).

  50. 50.

    Control mechanisms of polyphenic development in insects. BioScience 49, 181–192 (1999).

  51. 51.

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

  52. 52.

    Evolutionary morphology, innovation, and the synthesis of evolutionary and developmental biology. Biol. Philos. 18, 309–345 (2003).

  53. 53.

    & (eds) Evolutionary innovation and morphological novelty. J. Exp. Zool. B Mol. Dev. Evol. 304, Special issue (2005).

  54. 54.

    et al. The generation and diversification of butterfly eyespot color patterns. Curr. Biol. 11, 1578–1585 (2001).

  55. 55.

    & Evolutionary origin of insect wings from ancestral gills. Nature 385, 627–630 (1997).

  56. 56.

    , , & Cephalopod Hox genes and the origin of morphological novelties. Nature 424, 1061–1065 (2003).

  57. 57.

    , & Hox gene expression in teleost fins and the origin of vertebrate digits. Nature 375, 678–681 (1995).

  58. 58.

    Development and evolutionary origin of feathers. J. Exp. Zool. B Mol. Dev. Evol. 285, 291–306 (1999).

  59. 59.

    , , & Morphogenesis of the turtle shell: the development of a novel structure in tetrapod evolution. Evol. Dev. 3, 47–58 (2001).

  60. 60.

    & 'Generic' physical mechanisms of morphogenesis and pattern formation. Development 110, 1–18 (1990).

  61. 61.

    in From Embryology to Evo–Devo: A History of Embryology in the 20th Century (eds Laubichler, M. D. & Maienschein, J.) 499–524 (MIT Press, Cambridge, 2007).

  62. 62.

    & A gene network model accounting for development and evolution of mammalian teeth. Proc. Natl Acad. Sci. USA 99, 8116–8120 (2002).

  63. 63.

    , & The genetic basis of adaptive melanism in pocket mice. Proc. Natl Acad. Sci. USA 100, 5268–5273 (2003).

  64. 64.

    , & Evolution in black and white: genetic control of pigment patterns in Drosophila. Trends Genet. 19, 495–504 (2003).

  65. 65.

    Robustness and Evolvability in Living Systems (Princeton Univ. Press, Princeton, 2005).

  66. 66.

    , , & in Modeling Biology: Structures, Behaviors, Evolution (eds Laubichler, M. & Müller, G. B.) 355–378 (MIT Press, Cambridge, 2007).

  67. 67.

    Phenotypic Plasticity: Beyond Nature and Nurture (Johns Hopkins Univ. Press, Baltimore, 2001).

  68. 68.

    Reciprocal linkage between self-organizing processes is sufficient for self-reproduction and evolvability. Biol. Theor. 1, 136–149 (2006).

  69. 69.

    The Shape of Life (Chicago Univ. Press, Chicago, 1996).

  70. 70.

    The Development of Animal Form: Ontogeny, Morphology, and Evolution (Cambridge Univ. Press, Cambridge, 2003).

  71. 71.

    , & in Molecular Zoology (eds Ferraris, J. D. & Palumbi, S. R.) 267–295 (Wiley-Liss, New York, 1996).

  72. 72.

    & Developmental genetics and traditional homology. BioEssays 18, 489–494 (1996).

  73. 73.

    Molecules, developmental modules, and phenotypes: a combinatorial approach to homology. Mol. Phylogenet. Evol. 9, 340–347 (1997).

  74. 74.

    in Homology (eds Bock, G. R. & Cardew, G.) 189–203 (Wiley, Chichester, 1999).

  75. 75.

    The biological homology concept. Annu. Rev. Ecol. Syst. 20, 51–69 (1989).

  76. 76.

    & Larval ectoderm, organizational homology, and the origins of evolutionary novelty. J. Exp. Zool. B Mol. Dev. Evol. 306, 18–34 (2005).

  77. 77.

    & Evolution in Four Dimensions (MIT Press, Cambridge, 2005).

  78. 78.

    & Evolutionary modification of cell lineage in the direct-developing sea urchin Heliocidaris erythrogramma. Dev. Biol. 132, 458–470 (1989).

  79. 79.

    & Rapid evolution of gastrulation mechanisms in a sea urchin with lecithotrophic larvae. Evolution 45, 1741–1750 (1991).

  80. 80.

    Evolution of developmental mechanisms in nematodes. J. Exp. Zool. 285, 3–18 (1999).

  81. 81.

    & Evolution of nematode vulval fate patterning. Dev. Biol. 173, 396–407 (1996).

  82. 82.

    , & Before programs: the physical origination of multicellular forms. Int. J. Dev. Biol. 50, 289–299 (2006).

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Acknowledgements

The perspective of evo–devo represented in this article has greatly benefited from discussions with W. Callebaut, M. Laubichler, S. Newman, M. Pigliucci, J. Schwarz, G. P. Wagner and the members of my department.

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  1. Gerd B. Müller is at the Department of Theoretical Biology, University of Vienna, Althanstrasse 14 A-1090 Wien, Austria, and at the Konrad Lorenz Institute for Evolution and Cognition Research, A-3421 Altenberg, Austria.  gerhard.mueller@univie.ac.at

    • Gerd B. Müller

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Glossary

Canalization

The developmental buffering of phenotypic traits against genetic and environmental perturbations.

Generative bias

A tendency in the production of phenotypic variation or innovation that is caused by the properties of the developmental system.

Generic form

Biological forms that result from the autonomous interactions within and among cell aggregates, based on their physical properties, without a programme-like genetic control.

Genotype–phenotype map

A mathematical characterization of the correspondence of a set of genotypes with a set of phenotypes.

Heterochrony

Evolutionary changes in the timing of developmental events, such as the onset, offset or tempo of a process.

Homeotic transformation

The change of one body part into another, caused by a genetic or epigenetic perturbation of development.

Morphospace

A three-dimensional matrix of possible morphologies that is larger than the set of actual morphologies that are realized in nature.

Modern Synthesis

The prevailing theoretical framework of evolution that resulted from a combination of genetics, systematics, comparative morphology and palaeontology in the 1930s and 1940s. Also called Evolutionary Synthesis or Synthetic Theory.

Mechanochemical excitability

The capacity of cells to respond to physical and chemical stimuli.

Ontogeny

The course of individual development of an organism from the fertilized egg to the adult.

Phenocopy

An epigenetically induced phenotypic character that resembles a genetically determined character.

Polyphenism

Alternative phenotypes that arise from a single genotype as a result of differing environmental conditions.

Viscoelastic

Materials, such as cell masses, that have both viscous and elastic properties when they respond to strain.

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DOI

https://doi.org/10.1038/nrg2219

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