The "eyespot module" and eyespots as modules: development, evolution, and integration of a complex phenotype.

Organisms are inherently modular, yet modules also evolve in response to selection for functional integration or functional specialization of traits. For serially repeated homologous traits, there is a clear expectation that selection on the function of individual traits will reduce the integration between traits and subdivide a single ancestral module. The eyespots on butterfly wings are one example of serially repeated morphological traits that share a common developmental mechanism but are subject to natural and sexual selection for divergent functions. Here, I test two hypotheses about the organization of the eyespot pattern into independent dorsal-ventral and anterior-posterior modules, using a graphical modeling technique to examine patterns of eyespot covariation among and within wing surfaces in the butterfly Bicyclus anynana. Although there is a hierarchical and complex pattern of integration among eyespots, the results show a surprising mismatch between patterns of eyespot integration and the developmental and evolutionary eyespot units identified in previous empirical studies. These results are discussed in light of the relationships between developmental, functional, and evolutionary modules, and they suggest that developmental sources of independent trait variation are often masked by developmental sources of trait integration.

Allen CE 《-》

Developmental and genetic mechanisms for evolutionary diversification of serial repeats: eyespot size in Bicyclus anynana butterflies.

Serially repeated pattern elements on butterfly wings offer the opportunity for integrating genetic, developmental, and functional aspects towards understanding morphological diversification and the evolution of individuality. We use captive populations of Bicyclus anynana butterflies, an emerging model in evolutionary developmental biology, to explore the genetic and developmental basis of compartmentalized changes in eyespot patterns. There is much variation for different aspects of eyespot morphology, and knowledge about the genetic pathways and developmental processes involved in eyespot formation. Also, despite the strong correlations across all eyespots in one butterfly, B. anynana shows great potential for independent changes in the size of individual eyespots. It is, however, unclear to what extent the genetic and developmental processes underlying eyespot formation change in a localized manner to enable such individualization. We use micromanipulations of developing wings to dissect the contribution of different components of eyespot development to quantitative differences in eyespot size on one wing surface. Reciprocal transplants of presumptive eyespot foci between artificial selection lines and controls suggest that while localized antagonistic changes in eyespot size rely mostly on localized changes in focal signal strength, concerted changes depend greatly on epidermal response sensitivities. This potentially reflects differences between the signal-response components of eyespot formation in the degrees of compartmentalization and/or the temporal pattern of selection. We also report on the phenotypic analysis of a number of mutant stocks demonstrating how single alleles can affect different eyespots in concert or independently, and thus contribute to the individualization of serially repeated traits.

Beldade P ，French V ，Brakefield PM 《-》

Integration of wings and their eyespots in the speckled wood butterfly Pararge aegeria.

We investigated both the phenotypic and developmental integration of eyespots on the fore- and hindwings of speckled wood butterflies Pararge aegeria. Eyespots develop within a framework of wing veins, which may not only separate eyespots developmentally, but may at the same time also integrate them by virtue of being both signalling sources and barriers during eyespot development. We therefore specifically investigated the interaction between wing venation patterns and eyespot integration. Phenotypic covariation among eyespots was very high, but only eyespots in neighbouring wing cells and in homologous wing cells on different wing surfaces were developmentally integrated. This can be explained by the fact that the wing cells of these eyespots share one or more wing veins. The wing venation patterns of fore- and hindwings were highly integrated, both phenotypically and developmentally. This did not affect overall developmental integration of the eyespots. The adaptive significance of integration patterns is discussed and more specifically we stress the need to conduct studies on phenotypic plasticity of integration.

Breuker CJ ，Gibbs M ，Van Dyck H ，Brakefield PM ，Klingenberg CP ，Van Dongen S ... -  《JOURNAL OF EXPERIMENTAL ZOOLOGY PART B-MOLECULAR AND DEVELOPMENTAL EVOLUTION》

Eyespot evolution: phylogenetic insights from Junonia and related butterfly genera (Nymphalidae: Junoniini).

Butterfly eyespots have been the focus of a number of developmental and evolutionary studies. However, a phylogenetic component has rarely been explicitly incorporated in these studies. In this study, I utilize a phylogeny to trace the evolution of eyespot number and position on the wing in a group of nymphalid butterflies, the subtribe Junoniini. These butterflies have two kinds of eyespot arrangements which I refer to as Serial and Individual. In the Serial arrangement, eyespots are placed in a series on compartments 1-6 (counting from the anterior wing margin). In the Individual arrangement, eyespots are isolated on specific compartments, ranging from 1 to 4 in number. This can be divided into four subtypes based on the number and positions of eyespots. I map the evolution of these five arrangements over a phylogeny of Junoniini reconstructed with ca. 3000 base pairs of sequence data from three genes. The results show that almost all arrangements have evolved at least twice, with multiple shifts between them by addition and deletion of eyespots. I propose a model involving genetic or developmental coupling between eyespots in specific compartments to explain these shifts. I discuss their evolution in light of existing knowledge about their development. I also discuss potential explanations for functional significance of the eyespot patterns found in the group. Differential selection for and against eyespots, both at different times over the phylogeny and in different regions, have driven the evolution of eyespot arrangements. The study throws open many questions about the adaptive significance of eyespots and the developmental underpinnings of the various arrangements.

Kodandaramaiah U 《-》

Concerted evolution and developmental integration in modular butterfly wing patterns.

Developing organisms are thought to be modular in organization so that traits in different modules evolve independently whereas traits within a module change in a concerted manner. The eyespot pattern in Bicyclus anynana butterflies provides an ideal system where morphological modularity can be dissected and different levels of genetic integration analyzed. Several lines of evidence show that all eyespots in an individual butterfly are genetically integrated, suggesting that the whole pattern, rather than the separate eyespots, should be considered as a single character. However, despite the strong genetic correlations between the two eyespots on the dorsal forewing of B. anynana, there is great potential for independent changes. Here we use laboratory lines selected in different directions for the size of those eyespots to study correlated responses in the whole eyespot pattern. We show clear changes in eyespot size across all wing surfaces, which depend on eyespot position along the anterior-posterior axis. There are also changes in the number of extra eyespots and in eyespot color composition but no changes in eyespot position relative to wing margin. Our analysis of eyespot pattern modularity is discussed in the light of what is known about the cellular and genetic mechanisms of eyespot formation and the great potential for evolutionary diversification in butterfly wing patterns.

Beldade P ，Brakefield PM 《EVOLUTION & DEVELOPMENT》