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Altering the temporal regulation of one transcription factor drives sensory trade-offs

By Ariane Ramaekers, Simon Weinberger, Annelies Claeys, Martin Kapun, Jiekun Yan, Reinhard Wolf, Thomas Flatt, Erich Buchner, Bassem A Hassan

Posted 15 Jun 2018
bioRxiv DOI: 10.1101/348375 (published DOI: 10.1016/j.devcel.2019.07.027)

Size trade-offs of visual versus olfactory organs is a pervasive feature of animal evolution. Comparing Drosophila species, we find that larger eyes correlate with smaller antennae, where olfactory organs reside, and narrower faces. We demonstrate that this trade-off arises through differential subdivision of the head primordium into visual versus non-visual fields. Specification of the visual field requires a highly-conserved eye development gene called eyeless in flies and Pax6 in humans. We discover that changes in the temporal regulation of eyeless 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 that is sufficient to alter its temporal regulation and eye size. Because Pax6 is a conserved regulator of sensory placode subdivision, we propose that alterations in the mutual repression between sensory territories is a conserved mechanism for sensory trade-offs in animals.

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