Search

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.

We report a case of genetic linkage between the two major loci underlying different wing traits in the two-spot ladybird beetle, Adalia bipunctata (L.) (Coleoptera: Coccinellidae): melanism and winglessness. The loci are estimated to be 38.8 cM apart on one of the nine autosomes. This linkage is likely to facilitate the unravelling of the genetics of these traits. These traits are of interest in the context of the evolution of intraspecific morphological diversity, and for the application of ladybird beetles in biological control programs.

Modularity in animal development is thought to have facilitated morphological diversification, but independent change of those traits integrated within a module might be restricted. Correlations among traits describe potential developmental constraints on evolution. These have often been postulated to explain patterns of morphological variation and have been examined theoretically but seldom analyzed experimentally. Here, we use artificial selection to explore the modular organization of butterfly wing patterns and the extent to which their evolution is constrained by the genetic correlations among repeated pattern elements. We show that, in Bicyclus anynana butterflies, despite the evidence that all eyespots are developmentally coupled, the response to selection for increased size of one individual eyespot can proceed in a manner largely independent from selection imposed on another eyespot. We argue that among-eyespot correlations are unlikely to have constrained the evolutionary diversification of butterfly wing patterns but might be important when only limited time is available for adaptive evolution to occur. The ease with which we have been able to produce independent responses to artificial selection on different eyespots may be linked to a legacy of natural selection favoring individuality. Our results are discussed within the context of the evolution of modularity and individuality of serially repeated morphological traits.