Academic journal article Genetics

Patterning of the Adult Mandibulate Mouthparts in the Red Flour Beetle, Tribolium Castaneum

Academic journal article Genetics

Patterning of the Adult Mandibulate Mouthparts in the Red Flour Beetle, Tribolium Castaneum

Article excerpt

ABSTRACT Specialized insect mouthparts, such as those of Drosophila, are derived from an ancestral mandibulate state, but little is known about the developmental genetics of mandibulate mouthparts. Here, we study the metamorphic patterning of mandibulate mouthparts of the beetle Tribolium castaneum, using RNA interference to deplete the expression of 13 genes involved in mouthpart patterning. These data were used to test three hypotheses related to mouthpart development and evolution. First, we tested the prediction that maxillary and labial palps are patterned using conserved components of the leg-patterning network. This hypothesis was strongly supported: depletion of Distal-less and dachshund led to distal and intermediate deletions of these structures while depletion of homothorax led to homeotic transformation of the proximal maxilla and labium, joint formation required the action of Notch signaling components and odd-skipped paralogs, and distal growth and patterning required epidermal growth factor (EGF) signaling. Additionally, depletion of abrupt or pdm/nubbin caused fusions of palp segments. Second, we tested hypotheses for how adult endites, the inner branches of the maxillary and labial appendages, are formed at metamorphosis. Our data reveal that Distal-less, Notch signaling components, and odd-skipped paralogs, but not dachshund, are required for metamorphosis of the maxillary endites. Endite development thus requires components of the limb proximal-distal axis patterning and joint segmentation networks. Finally, adult mandible development is considered in light of the gnathobasic hypothesis. Interestingly, while EGF activity is required for distal, but not proximal, patterning of other appendages, it is required for normal metamorphic growth of the mandibles.

SPECIALIZED insect mouthparts are derived from an ancestral mandibulate state, with chewing mandibles and maxillary and labial palps. Little is known about the patterning of mandibulate mouthparts. Through functional study of 13 genes in the beetle Tribolium castaneum, we examine patterning in mandibulate mouthparts and test several hypotheses about the evolution of insect mouthparts. The maxillae and labium in this beetle share many patterning features with legs. Endites, the inner mouthpart branches, require the same genes involved in axial patterning and joint formation. Intriguingly, the mandibles of T. castaneum, which evolved through loss of distal identity, nonetheless require epidermal growth factor (EGF) signaling, which is required for development of distal regions of other appendages.

Arthropods share a body plan of serially homologous body segments (Snodgrass 1928; Brusca et al. 2002; Boxshall 2004). Within this body plan a great diversity of forms has been generated in several ways, including changes in the number of body segments, patterns of regionalization (tagmosis), and appendage morphology. While insects are the most diverse arthropod group in terms of species numbers, they have a fixed pattern of tagmosis and little variation in the number of body segments (Brusca et al. 2002). Diversification of appendage morphology, however, has played a key role in the diversification of insects; mouthpart morphology is especially variable across lineages, which has enabled exploitation of diverse dietary niches.

Early insects evolved a generalized set of mouthparts useful in biting, chewing, and manipulation of food. Over the last 350 million years, insect mouthparts diversified along with new food sources, and many specialized mouthparts have been derived from the ancestral mandibulate form (Grimaldi and Engel 2005). Some examples of mouthpart specializations include the piercing stylets and beak of bugs (Hemiptera), the elongated galea tubes used by Lepidoptera in nectar feeding, and the sponging proboscis of brachyceran flies. The developmental genetics of several of these specialized mouthparts have been studied (Abzhanov et al. …

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