Co‐option of the eye developmental gene regulatory network may have led to the appearance of novel functional traits on the wings of flies and butterflies. The first trait is a recently described wing organ in a species of extinct midge resembling the outer layers of the midge's own compound eye. The second trait is red pigment patches on Heliconius butterfly wings connected to the expression of an eye selector gene, optix. These examples, as well as others, are discussed regarding the (...) type of empirical evidence and burden of proof that have been used to infer gene network co‐option underlying the origin of novel traits. A conceptual framework describing increasing confidence in inference of network co‐option is proposed. Novel research directions to facilitate inference of network co‐option are also highlighted, especially in cases where the pre‐existent and novel traits do not resemble each other. (shrink)

Co‐option of the eye developmental gene regulatory network may have led to the appearance of novel functional traits on the wings of flies and butterflies. The first trait is a recently described wing organ in a species of extinct midge resembling the outer layers of the midge's own compound eye. The second trait is red pigment patches on Heliconius butterfly wings connected to the expression of an eye selector gene, optix. These examples, as well as others, are discussed regarding the (...) type of empirical evidence and burden of proof that have been used to infer gene network co‐option underlying the origin of novel traits. A conceptual framework describing increasing confidence in inference of network co‐option is proposed. Novel research directions to facilitate inference of network co‐option are also highlighted, especially in cases where the pre‐existent and novel traits do not resemble each other. (shrink)

Serial homology is widespread in organismal design, but the origin and individuation of these repeated structures appears to differ with the different types of serial homologues, and remains an intriguing and exciting topic of research. Here I focus on the evolution of the serially repeated eyespots that decorate the margin of the wings of nymphalid butterflies. In this system, unresolved questions relate to the evolutionary steps that lead to the appearance of these serial homologues and how their separate identities evolved. (...) I present and discuss two alternative hypotheses. The first proposes that eyespots first appeared as a row of undifferentiated repeated modules, one per wing compartment, that later become individuated. This individuation allowed eyespots to appear and disappear from specific wing compartments and also allowed eyespots to acquire different morphologies. The second hypothesis proposes that eyespots first appeared as individuated single units, or groups of units, that over evolutionary time were co‐opted into new compartments on the wing. I discuss the merits of each of these alternate hypotheses by finding analogies to other systems and propose research avenues for addressing these issues in the future. BioEssays 30:358–366, 2008. © 2008 Wiley Periodicals, Inc. (shrink)

The differentiation of male and female characteristics in vertebrates and insects has long been thought to proceed via different mechanisms. Traditionally, vertebrate sexual development was thought to occur in two phases: a primary and a secondary phase, the primary phase involving the differentiation of the gonads, and the secondary phase involving the differentiation of other sexual traits via the influence of sex hormones secreted by the gonads. In contrast, insect sexual development was thought to depend exclusively on cell‐autonomous expression of (...) sex‐specific genes. Recently, however, new evidence indicates that both vertebrates and insects rely on sex hormones as well as cell‐autonomous mechanisms to develop sexual traits. Collectively, these new data challenge the traditional vertebrate definitions of primary and secondary sexual development, call for a redefinition of these terms, and indicate the need for research aimed at explaining the relative dependence on cell‐autonomous versus hormonally guided sexual development in animals. (shrink)

The particular fascination of butterfly wings for developmental biologists (and others) lies in their spectacular array of colour patterns. The evolutionary and developmental relationships between these patterns have been analysed and we know something of the cell interactions involved in their formation(1). Now butterfly homologues of Drosophila wing‐patterning genes have been identified, and their expression patterns offer the first clues to the molecular mechanisms which specify wing colour patterns(2).

In this paper we describe a test for Nijhout's hypothesis that the eyespot patterns on butterfly wings are the result of a threshold reaction of the epidermal cells to a concentration gradient of a diffusing degradable morphogen produced by focal cells at the centre of the future eyespot. The wings of the nymphalid butterfly, Bicyclus anynana, have a series of eyespots, each composed of a white pupil, a black disc and a gold outer ring. In earlier extirpation and transplantation experiments (...) it has been established that these eyespots are indeed organised around groups of signalling cells active during the first hours of pupal development. If these cells were to supply the positional information for eyespot formation in accordance with Nijhout's diffusion-degradation gradient model, then, when two foci are close together, the signals should sum, and this effect should be apparent in the detailed shape of the resulting pigment pattern. We give an equation for the form of the contours that would be obtained in this manner. We use this to test the morphogen gradient hypothesis on measurements of the outlines of fused eyespots obtained either by grafting focal cells close together, or by using a mutation that produces adjacent fused eyespots. The contours of the fused patterns were found to satisfy our equation, thus corroborating Nijhout's hypothesis to the extent possible with this particular type of experiment. (shrink)

One of the central but yet unresolved problems in evolutionary biology concerns the origin of novel complex traits. One hypothesis is that complex traits derive from pre‐existing gene regulatory networks (GRNs) reused and modified to specify a novel trait somewhere else in the body. This simple explanation encounters problems when the novel trait that emerges in a body is in a region that is known to harbor a latent or repressed trait that has been silent for millions of years. Is (...) the novel trait merely a re‐emerged de‐repressed trait or a truly novel trait that emerged via a novel deployment of an old GRN? A couple of new studies sided on opposite sides of this question when investigating the origin of horns in dung beetles and helmets in treehoppers that develop in the first thoracic segment (T1) of their bodies, a segment known to harbor a pair of repressed/modified wings in close relatives. Here, I point to some key limitations of the experimental approaches used and highlight additional experiments that could be done in future to resolve the developmental origin of these and other traits. (shrink)