Butterfly wings shaped by a molecular cookie cutter: evolutionary radiation of lepidopteran wing shapes associated with a derived Cut/wingless wing margin boundary system.

Butterflies and moths show a remarkable diversity of specialized wing shapes, yet little is known about the molecular basis of wing shape determination. To learn more about this process we examined the expression of dorsoventral (DV) boundary candidate genes in developing wings of several species of Lepidoptera. We found that the transcription factor Cut and mRNA for the signaling molecule wingless (wg) are strongly co-expressed in a discrete zone around the larval wing disc margin. Surprisingly, the expression boundary of Cut and wg clearly presages complex future adult wing shapes, including the hindwing tails of swallowtail butterflies, very early in final-instar wing disc development. During pupal wing development the cells in this zone undergo apoptosis, thereby defining the actual margin of the adult wing. Comparison with gene expression in beetle and fly wings suggests that this delineation of a topologically independent boundary running parallel to the DV boundary is a derived feature of Lepidoptera. We propose that the developmental decoupling of wing margin determination and DV boundary formation was a major developmental innovation that facilitated the radiation of specialized wing shapes in moths and butterflies.