Capturing embryonic development from metamorphosis: how did the terminal patterning signalling pathway of Drosophila evolve?

Abstract

The Torso receptor tyrosine kinase has two crucial roles in Drosophila melanogaster development. One is in the control of insect moulting, which is regulated by the neuropeptide hormone PTTH (prothoracicotropic hormone). PTTH activates ERK signalling via Torso in the prothoracic gland to stimulate ecdysone secretion. Torso also has a role in control of one of the earliest events in embryogenesis in Drosophila; patterning of the embryonic termini. Here Torso is activated by a different, but related, peptide called Trunk. During terminal patterning another protein, Torso-like, has a key role in mediating activation of Torso by Trunk. Torso-like is also expressed in the prothoracic gland and null-mutants have defective developmental timing in Drosophila. This function, however, has been recently shown to be independent of Torso and PTTH. We refer to these proteins, Trunk, PTTH, Torso and Torso-like, as the Torso-activation module. Outside Drosophila we see that the genes encoding the Torso-activation module have a complex phylogenetic history, with different origins and multiple losses of components of this signalling pathway during arthropod evolution. This, together with expression and functional data in a range of insects, leads us to propose that the terminal patterning pathway in Drosophila and Tribolium arose through co-option of PTTH/Trunk and Torso, which has a role in developmental timing, into a new context, and that Torso-like was recruited specifically in the ovary to modulate the specificity of this pathway.