bric à brac (bab), a central player in the gene regulatory network that mediates thermal plasticity of pigmentation in Drosophila melanogaster

Drosophila body pigmentation has emerged as a major Evo-Devo model. Using two Drosophila melanogaster lines, Dark and Pale, selected from a natural population, we analyse here the interaction between genetic variation and environmental factors to produce this complex trait. Indeed, pigmentation varies with genotype in natural populations and is sensitive to temperature during development. We demonstrate that the bric à brac (bab) genes, that are differentially expressed between the two lines and whose expression levels vary with temperature, participate in the pigmentation difference between the Dark and Pale lines. The two lines differ in a bab regulatory sequence, the dimorphic element (called here bDE). Both bDE alleles are temperature-sensitive, but the activity of the bDE allele from the Dark line is lower than that of the bDE allele from the Pale line. Our results suggest that this difference could partly be due to differential regulation by AbdB. bab has been previously reported to be a repressor of abdominal pigmentation. We show here that one of its targets in this process is the pigmentation gene tan (t), regulated via the tan abdominal enhancer (t_MSE). Furthermore, t expression is strongly modulated by temperature in the two lines. Thus, temperature sensitivity of t expression is at least partly a consequence of bab thermal transcriptional plasticity. We therefore propose that a gene regulatory network integrating both genetic variation and temperature sensitivity modulates female abdominal pigmentation. Interestingly, both bDE and t_MSE were previously shown to have been recurrently involved in abdominal pigmentation evolution in drosophilids. We propose that the environmental sensitivity of these enhancers has turned them into evolutionary hotspots.