Altering the Temporal Regulation of One Transcription Factor Drives Evolutionary Trade-Offs between Head Sensory Organs

Ariane Ramaekers, Annelies Claeys, Martin Kapun, Emmanuèle Mouchel-Vielh, Delphine Potier, Simon Weinberger, Nicola Grillenzoni, Delphine Dardalhon-Cuménal, Jiekun Yan, Reinhard Wolf, Thomas Flatt, Erich Buchner, Bassem A Hassan 


Size trade-offs of visual versus olfactory organs is a pervasive feature of animal evolution. This could result from genetic or functional constraints. We demonstrate that head sensory organ size trade-offs in Drosophila are genetically encoded and arise through differential subdivision of the head primordium into visual versus non-visual fields. We discover that changes in the temporal regulation of the highly conserved eyeless/Pax6 gene expression during development is a conserved mechanism for sensory trade-offs within and between Drosophila species. We identify a natural single nucleotide polymorphism in the cis-regulatory region of eyeless in a binding site of its repressor Cut that is sufficient to alter its temporal regulation and eye size. Because eyeless/Pax6 is a conserved regulator of head sensory placode subdivision, we propose that its temporal regulation is key to define the relative size of head sensory organs.


DOI: 10.1016/j.devcel.2019.07.027