Multiple gene co-options underlie the rapid evolution of sexually deceptive flowers in Gorteria diffusa

Gene co-option, the redeployment of an existing gene in an unrelated developmental context, is an important mechanism underlying the evolution of morphological novelty. In most cases described to date, novel traits emerged by co-option of a single gene or genetic network. Here, we show that the integration of multiple co-opted genetic elements facilitated the rapid evolution of complex petal spots that mimic female bee-fly pollinators in the sexually deceptive South African daisy Gorteria diffusa. First, co-option of iron homeostasis genes altered petal spot pigmentation, producing a color similar to that of female pollinators. Second, co-option of the root hair gene GdEXPA7 enabled the formation of enlarged papillate petal epidermal cells, eliciting copulation responses from male flies. Third, co-option of the miR156-GdSPL1 transcription factor module altered petal spot placement, resulting in better mimicry of female flies resting on the flower. The three genetic elements were likely co-opted sequentially, and strength of sexual deception in different G. diffusa floral forms strongly correlates with the presence of the three corresponding morphological alterations. Our findings suggest that gene co-options can combine in a modular fashion, enabling rapid evolution of novel complex traits. •Co-option of iron homeostasis, root hair, and phase transition genes in petal spots•Co-options change coloration, cell structure, and placement of petal spots•Altered petal spots mimic female flies and enable pollination by sexual deception•Integration of multiple gene co-options facilitates the evolution of novel traits Using an integrative evo-devo approach, Kellenberger et al. show that three independent gene co-options altering the color, structure, and placement of petal spots underlie the evolution of sexual deception in the daisy Gorteria diffusa. This work shows that gene co-options can combine in a modular way, giving rise to complex phenotypic novelties.