Evolution of insect abdominal appendages: Are prolegs homologous or convergent traits?

Abstract

Many insects possess abdominal prolegs, raising the question of whether these prolegs are homologous or convergent structures. One way to address this issue is to compare mechanisms controlling the development of prolegs in different insects. Segmental morphologies along the insect body are controlled by the regulatory activities of the Hox proteins, and one well-studied regulatory target is the Distal-less (Dll) gene, which is required for the development of distal limb structures in arthropods. In Drosophila abdominal segments, Dll transcription is prevented by Hox proteins of the Bithorax Complex (BX-C). In lepidopteran abdominal segments, circular holes lacking BX-C protein expression allow Dll to be expressed and prolegs to develop. For comparison, we examined protein expression patterns in two species of sawfly from the hymenopteran suborder Symphyta; these insects develop prolegs on all abdominal segments. Interestingly, sawfly prolegs did not express Dll protein at any time, and expressed BX-C proteins throughout development. These results suggest that sawfly prolegs lack distal elements that are present in lepidopteran prolegs. Consistent with this interpretation, the proximal determinant extradenticle (exd) was present in cell nuclei all of the way to the tip of the sawfly proleg, whereas it was not detectable in the nuclei of cells near the tip of the lepidopteran proleg. Our results support the hypothesis that larval prolegs have evolved independently in the Lepidoptera and Hymenoptera.