Segmental identity of caudal cuticular features of Drosophila melanogaster larvae and its control by the bithorax complex

Abstract

This investigation examines the segmental origins of cuticular features of the caudal larva, and the effect on caudal development of mutations and deficiencies of the bithorax complex (BX-C). The posterior tip of the larva is formed by the fusion of abdominal segment 8 (AB8) with two more posterior segments which are presumably abdominal segments 9 and 10; we will refer to the derivatives of AB9 and AB10 as the “telson.” The caudal tip is rich in cuticular features, but their segmental origin is in many cases uncertain. We have analyzed the cuticular morphology of embryos homozygous for “pair-rule” mutations at the paired, odd-skipped, even-skipped, or hairy genes, which cause pattern deletions reiterated along the anterior-posterior axis. By correlating aberrant cuticle patterns in the thorax to those in the telson, we have been able to assign the segmental origin of cuticular features of the telson. This study suggests that AB8 elaborates three pairs of sensilla (the two anterior-most and the dorsal-most pairs), the posterior spiracle and its Filzkorper, and spinule groups both anterior and posterior to the spiracles. The lateral three pairs of sensilla belong to AB9, whereas the anal pads and the ventral pair of sensilla are formed by AB10. Previous studies have indicated that Df(3R)P9 deletes the entire BX-C, and when homozygous results in lethal embryos displaying homoeotic abnormalities in a region extending from the posterior mesothorax through the telson. Studies by others have shown that the centromere-proximal genetic domain of the BX-C (the Ultrabithorax-bithoraxoid region) controls developmental decisions in portions of the thorax and first abdominal segment, whereas the more distal abdominal-A ( abd-A, also called iab-2) and Abdominal-B ( Abd-B, or iab-7) mutations result in homoeotic changes in the abdomen. We have studied the cuticular morphology of the caudal segments of lethal zygotes lacking portions of the BX-C and of hemizygotes for BX-C mutations. We have observed that the developmental abnormalities of abd-A and Abd-B are restricted to a region anterior to what appears (based on studies of pair-rule mutants) to represent the anterior-posterior compartment boundary of AB8. This observation is consistent with the suggestion that BX-C genes are regulated within developmental units (more recently termed parasegments) comprised of the posterior region of one segment and the contiguous anterior region of the adjacent segment. We have confirmed that lethal larvae hemizygous for lethal right of bithorax (which lies distally in the region deleted by Df(3R)P9) appear cuticularly normal. We suggest that the distal BX-C includes both an abdominal domain including the abd-A + and Abd-B + (or iab-2 + through iab-7 +) functions and an additional domain (for which no loss of function mutations have been reported) necessary for the normal development of the posterior AB8 and the telson.