Conservation and diversification of gene function during mouthpart development in Onthophagus beetles

Abstract

The evolutionary success of insects is in part attributable to the tremendous diversification of their mouthparts, which permitted insects to radiate into novel food niches. The developmental genetic basis of mouthpart development has been well studied in at least two insect taxa possessing derived mouthparts, the hemipteran Oncopeltus fasciatus and Drosophila. However, much less is known about the regulation of mouthpart differentiation of the presumed ancestral mandibulate type. Here we aim to extend current insights into the patterning of mandibulate mouthparts through a functional genetic analysis of three leg gap genes, homothorax (hth), dachshund (dac), and Distal-less (Dll), in the dung beetle Onthophagus taurus, a species whose mouthpart arrangement has in part retained, as well as diverged form, the ancestral mandibulate mouthpart type. We specifically include in this study a first functional genetic analysis of the adult labrum, an enigmatic mouthpart whose appendicular origin has been the subject of a long-standing debate. Our results support a functional role of all three patterning genes in the development of the labium, maxilla, as well as the labrum. In contrast, mandible development appeared to rely only on the patterning functions of hth and dac, but not Dll. Here, our results raise the possibility that evolutionary changes in the dac-patterning may have played an important role in the evolutionary transition from a short, triangular mandible adapted for chewing to the elongated, flat, and blade-like mandible of modern filter-feeding scarabaeine beetles. In general, our results contribute to a growing body of studies that suggest that basic patterning genes can contribute to morphological evolution of adult features while maintaining traditional patterning responsibilities at earlier developmental stages or in other body regions.