Developmental and evolutionary implications of labial, Deformed and engrailed expression in the Drosophila head

Abstract

Prior developmental genetic analyses have shown that labial (lab) and Deformed (Dfd) are homeotic genes that function in the development of the embryonic (larval) and adult head. Using antibody probes to reveal the spatial distribution of the lab and Dfd proteins in embryonic and imaginal tissues, we have assessed the respective roles of these genes through an analysis of the correspondence of their expression patterns with their mutant phenotypes. With regard to imaginal development, lab and Dfd occupy adjacent non-overlapping expression domains in the peripodial cell layer of the eye-antennal disc, in patterns that are consistent with their adult mutant phenotypes and published fate maps. During embryogenesis, lab and Dfd exhibit limited overlapping expression in areas that are of no obvious significance to the development of larval head structures, but also in areas that may have consequences for imaginal development. The head of Drosophila and other cyclorrhaphous Dipterans is characterized by an extreme morphological difference between the larval and adult stages. Given this unique ontogenetic and phylogenetic history and the observation that homeotic transformations produced by the lab, Dfd, and proboscipedia (pb) loci are manifested only in the adult, we suggest that distinct regulatory paradigms evolved for homeotic gene function in the development of the larval versus adult head. Finally, a detailed examination of the engrailed (en) expression pattern in the embryonic head strengthens the view of insect morphologists that the clypeolabrum evolved from the fusion of paired labral appendages.