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Developmental constraints versus flexibility in morphological evolution

Nature volume 416, pages 844847 (25 April 2002) | Download Citation

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Abstract

Evolutionary developmental biology has encouraged a change of research emphasis from the sorting of phenotypic variation by natural selection to the production of that variation through development1. Some morphologies are more readily generated than others, and developmental mechanisms can limit or channel evolutionary change2. Such biases determine how readily populations are able to respond to selection3, and have been postulated to explain stasis in morphological evolution4 and unexplored morphologies5. There has been much discussion about evolutionary constraints6,7,8 but empirical data testing them directly are sparse9,10. The spectacular diversity in butterfly wing patterns11 is suggestive of how little constrained morphological evolution can be. However, for wing patterns involving serial repeats of the same element, developmental properties suggest that some directions of evolutionary change might be restricted12,13. Here we show that despite the developmental coupling between different eyespots in the butterfly Bicyclus anynana, there is great potential for independent changes. This flexibility is consistent with the diversity of wing patterns across species and argues for a dominant role of natural selection, rather than internal constraints, in shaping existing variation.

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References

  1. 1.

    Perspective: Evolutionary developmental biology and the problem of variation. Evolution 54, 1079–1091 (2000).

  2. 2.

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

  3. 3.

    The influence of variation and development constraints on the rate of multivariate phenotypic evolution. J. Evol. Biol. 1, 45–66 (1988).

  4. 4.

    in Rates of Evolution (eds Campbell, K. S. W. & Day, M. F.) (Allen & Unwin, London, 1987).

  5. 5.

    A developmental constraint in Cerion, with comments on the definition and interpretation of constraint in evolution. Evolution 43, 516–539 (1989).

  6. 6.

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

  7. 7.

    & Ontocogenophyloconstraints? The chaos of constraint terminology. Trends Ecol. Evol. 6, 166–168 (1991).

  8. 8.

    & The fall and rise of Dr Pangloss: adaptationism and the Spandrels paper 20 years later. Trends Ecol. Evol. 15, 66–70 (2000).

  9. 9.

    , & Experimental tests of the role of adaptation, chance, and history in evolution. Science 267, 87–90 (1995).

  10. 10.

    & Variability in the reversibility of evolution. Nature 408, 463–466 (2000).

  11. 11.

    The Development and Evolution of Butterfly Wing Patterns (Smithsonian Inst. Press, Washington, 1991).

  12. 12.

    The evolution–development interface and advances with the eyespot patterns in Bicyclus butterflies. Heredity 80, 265–272 (1998).

  13. 13.

    Structure of a character and the evolution of butterfly eyespot patterns. J. Exp. Zool. 291, 93–104 (2001).

  14. 14.

    Symmetry systems and compartments in lepidopteran wings—the evolution of a patterning mechanism. Development (Suppl.) 225–233 (1994).

  15. 15.

    & Phenotypic correlation structure among elements of the color pattern in Precis coenia (Lepidoptera, Nymphalidae). Evolution 47, 593–618 (1993).

  16. 16.

    , & The evolutionary genetics and developmental basis of wing pattern variation in the butterfly Bicyclus anynana. Evolution 48, 1147–1157 (1994).

  17. 17.

    Quantitative genetics and developmental constraints on evolution by selection. J. Theor. Biol. 110, 155–171 (1984).

  18. 18.

    Quantitative genetics of butterfly wing color patterns. Dev. Genet. 15, 79–91 (1994).

  19. 19.

    & Eyespot development on butterfly wings: the focal signal. Dev. Biol. 168, 112–123 (1995).

  20. 20.

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

  21. 21.

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

  22. 22.

    , & Contribution of Distal-less to quantitative variation in butterfly eyespots. Nature 415, 315–318 (2002).

  23. 23.

    , & Butterfly eyespots: the genetics and development of the color rings. Evolution 51, 1207–1216 (1997).

  24. 24.

    in Organisational Constraints on the Dynamics of Evolution (eds Vida, G. & Maynard-Smith, J.) 197–210 (Manchester Univ. Press, 1983).

  25. 25.

    How small are the smallest selectable domains of form?Genetics 130, 345–353 (1992).

  26. 26.

    Biostatistical Analysis (Prentice Hall, Upper Saddle River, 1999).

  27. 27.

    Evolutionary Quantitative Genetics (Chapman & Hall, New York, 1999).

  28. 28.

    Independent development of homologous pattern elements in the wing patterns of butterflies. Dev. Biol. 108, 146–151 (1985).

  29. 29.

    & Limits to natural selection. BioEssays 22, 1075–1084 (2000).

  30. 30.

    Monographie du Genre Bicyclus (Lepidoptera, Satyridae) (Inst. Fond. Afr. Noire, Dakar, 1973).

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Acknowledgements

We thank V. French, M. Matos, H. Metz, H. Teotónio, G. Wagner and B. Zwaan for helpful discussions about the experimental design, M. Lavrijsen, E. Schlatmann, B. de Winter and N. Wurzer for cultivating maize for hungry larvae, and V. French and H. Teotónio for comments on the manuscript. This work was supported by the Portuguese Foundation for Science and Technology under the Gulbenkian PhD Program (P.B.) and the Human Frontiers Science Program (P.M.B.).

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  1. *Institute of Evolutionary and Ecological Sciences, Leiden University, PO Box 9516, 2300 RA Leiden, The Netherlands

    • PatrÍcia Beldade
    • , Kees Koops
    •  & Paul M. Brakefield

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The authors declare that they have no competing financial interests

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Correspondence to PatrÍcia Beldade.

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https://doi.org/10.1038/416844a

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