Patterning of the adult mandibulate mouthparts in the red flour beetle, Tribolium castaneum

• Published in: Genetics (Austin) 2012-02, Vol.190 (2), p.639-654
• Main Authors: Angelini, David R, Smith, Frank W, Aspiras, Ariel C, Kikuchi, Moto, Jockusch, Elizabeth L
• Format: Article
• Language: English
• Subjects: Animals; Body Patterning - genetics; ErbB Receptors - metabolism; Genes, Insect; Genetics; Homeodomain Proteins - genetics; Insects; Investigations; Ligands; Mandible - anatomy & histology; Mandible - growth & development; Mandible - metabolism; Maxilla - anatomy & histology; Maxilla - growth & development; Maxilla - metabolism; Metamorphosis, Biological - genetics; Morphology; Nuclear Proteins - genetics; Phenotype; Receptors, Notch - metabolism; Ribonucleic acid; RNA; RNA Interference; RNA, Double-Stranded - metabolism; Signal Transduction; Tribolium - genetics; Tribolium - growth & development; Zinc Fingers - genetics
• ISSN: 1943-2631; 0016-6731; 1943-2631
• DOI: 10.1534/genetics.111.134296

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.