The evolution of abdominal reduction and the recent origin of distinct Abdominal-B transcript classes in Diptera

In insects, the Hox gene Abdominal-B (Abd-B) governs the development of the posterior-most segments, the number and fate of which differ within and between orders. A striking feature of insect evolution is a trend toward the reduction of posterior abdominal segments which is most pronounced in higher Diptera. In Drosophila melanogaster, two distinct Abd-B transcript classes and protein isoforms are expressed in non-overlapping domains and have discrete functions in patterning the posterior abdomen. It has been proposed that evolutionary changes in Abd-B structure and expression are responsible for the reduction of the dipteran abdomen. We have investigated the relationship between the evolution of the Abd-B gene and abdominal reduction by analyzing the structure and expression of homologs from four additional dipterans representing distinct clades within the order. The lower dipteran mosquito Anopheles gambiae expresses a single Abd-B transcript class, as do two species phylogenetically intermediate to mosquitoes and drosophilids. These results delimit the evolution of distinct functional Abd-B isoforms to within the dipteran radiation after the origin of the reduced abdominal morphology. Furthermore, we found that the spatial distribution of Abd-B transcripts in non-drosophilid Diptera is identical to the combined domains of the two D. melanogaster Abd-B transcripts. Therefore, neither the structural evolution nor changes in the spatial regulation of Abd-B account for the derived abdomen of higher Diptera. The recent subfunctionalization of this Hox gene has occurred without any apparent morphological correlate. We conclude that regulatory modifications to developmental programs downstream of or parallel to Abd-B are responsible for the evolutionary reduction of the higher dipteran postabdomen.