Shifting roles of Drosophila pair-rule gene orthologs: Segmental expression and function in the milkweed bug Oncopeltus fasciatus

Abstract

The discovery of pair-rule genes (PRGs) in Drosophila revealed the existence of an underlying two-segment-wide prepattern directing embryogenesis. The milkweed bug Oncopeltus fasciatus, a hemimetabolous insect, is a more representative arthropod: most of its segments form sequentially after gastrulation. Here, we report the expression and function of orthologs of the complete set of nine Drosophila PRGs in Oncopeltus. Seven Of-PRG-orthologs are expressed in stripes in the primordia of every segment, rather than every other segment; Of-runt is PR-like and several orthologs are also expressed in the segment addition zone. RNAi-mediated knockdown of Of-odd-skipped, paired and sloppy-paired impacted all segments, with no indication of PR-like register. We confirm that Of-E75A is expressed in PR-like stripes, although it is not expressed in this way in Drosophila, demonstrating the existence of an underlying PR-like prepattern in Oncopeltus. These findings reveal that a switch occurred in regulatory circuits, leading to segment formation: while several holometabolous insects are ‘Drosophila-like’, using PRG orthologs for PR patterning, most Of-PRGs are expressed segmentally in Oncopeltus, a more basally branching insect. Thus, an evolutionarily stable phenotype – segment formation – is directed by alternate regulatory pathways in diverse species.