Specification of the endocrine primordia controlling insect moulting and metamorphosis by the JAK/STAT signalling pathway

The corpora allata and the prothoracic glands control moulting and metamorphosis in insects. These endocrine glands are specified in the maxillary and labial segments at positions homologous to those forming the trachea in more posterior segments. Glands and trachea can be homeotically transformed into each other suggesting that all three evolved from a metamerically repeated organ that diverged to form glands in the head and respiratory organs in the trunk. While much is known about tracheal specification, there is limited information about corpora allata and prothorathic gland specification. Here we show that the expression of a key regulator of early gland development, the snail gene, is controlled by the Dfd and Scr Hox genes and by the Hedgehog and Wnt signalling pathways that induce localised transcription of upd, the ligand of the JAK/STAT signalling pathway, which lies at the heart of gland specification. Our results show that the same upstream regulators are required for the early gland and tracheal primordia specification, reinforcing the hypothesis that they originated from a segmentally repeated organ present in an ancient arthropod. Author summary The main endocrine organs controlling insect moulting and metamorphosis are the corpora allata and the prothoracic glands. Genetic experiments in Drosophila melanogaster suggested that, despite their extremely different morphology and function, the corpora allata and the prothoracic glands are homologous to the respiratory trachea. All three organs derive from a primordium arising at similar locations along the cephalic and trunk segments, they activate common developmental genes using the same cis-regulatory elements, and can be transformed into each other by modifying Hox expression. One key difference between glands and trachea is that the endocrine primordia activate the Epithelial to Mesenchymal inducer gene snail. Using the snail gland specific enhancer as a proxy for gland formation, we show that the glands are specified by the same inputs specifying the trachea. These include the JAK/STAT, the Hedgehog and Wingless signalling pathways as well as inputs from the Hox genes. These observations support the hypothesis that during arthropod evolution, a metamerically repeated organ diverged to give rise to endocrine glands in the head and respiratory organs in the trunk segments.

Automated summary

The corpora allata and the prothoracic glands control moulting and metamorphosis in insects. These endocrine glands are regulated by the same upstream genes, supporting the hypothesis that they originated from a repeated organ.