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Developmental constraints versus flexibility in morphological evolution

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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Figure 1: Response to artificial selection on the size of the dorsal forewing eyespots of B. anynana.
Figure 2: Response to relaxed selection (G11–G19) and additional directional selection (G19–G25).
Figure 3: Diversity of eyespot patterns across the genus Bicyclus.

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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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Correspondence to PatrÍcia Beldade.

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Beldade, P., Koops, K. & Brakefield, P. Developmental constraints versus flexibility in morphological evolution. Nature 416, 844–847 (2002). https://doi.org/10.1038/416844a

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