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

Abstract

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.

Seasonal plasticity in anti-predatory strategies: matching of color and color preference for effective crypsis

“…Traits making up the B. anynana seasonal syndrome, including eyespot size ), life-history traits , and courtship behavior (Bear et al 2017), are known to be affected by developmental temperature-dependent ecdysteroid hormone dynamics during the late-larval and early pupal stages. How ecdysone dynamics can affect the biosynthetic pathways for pigment production in B. anynana (Beldade and Peralta 2017;Zhang et al 2017) is unclear, but effects of developmental temperature on these pathways have been studied in detail in Drosophila melanogaster (Gibert et al 2007(Gibert et al , 2017De Castro et al 2018), a well-described model for thermal plasticity in body pigmentation. Studies in other systems have also shown how temperature-induced changes in ecdysteroid signaling can affect adult behavior in different manners: by altering neuronal activity and connectivity (e.g.…”

Seasonal plasticity in anti-predatory strategies: Matching of color and color preference for effective crypsis

“…, ; De Castro et al. ), a well‐described model for thermal plasticity in body pigmentation. Studies in other systems have also shown how temperature‐induced changes in ecdysteroid signaling can affect adult behavior in different manners: by altering neuronal activity and connectivity (e.g., in D. melanogaster ; Ishimoto et al.…”

“…Traits making up the B. anynana seasonal syndrome, including eyespot size , life-history traits , and courtship behavior (Bear et al 2017), are known to be affected by developmental temperature-dependent ecdysteroid hormone dynamics during the late-larval and early pupal stages. How ecdysone dynamics can affect the biosynthetic pathways for pigment production in B. anynana (Beldade and Peralta 2017;Zhang et al 2017) is unclear, but effects of developmental temperature on these pathways have been studied in detail in Drosophila melanogaster (Gibert et al 2007(Gibert et al , 2017De Castro et al 2018), a well-described model for thermal plasticity in body pigmentation. Studies in other systems have also shown how temperature-induced changes in ecdysteroid signaling can affect adult behavior in different manners: by altering neuronal activity and connectivity (e.g., in D. melanogaster; Ishimoto et al 2013;Carvalho and Mirth 2015) and/or by mediating visual sensitivity of adults through the regulation of eye development (e.g., in Manduca sexta; Champlin and Truman 1998).…”

Genomics of Developmental Plasticity in Animals

“…Detailed studies of specific and well-known developmental pathways in emblematic plasticity models, such as pigmentation in Drosophila (e.g. De Castro et al, 2018), body and organ size in different insects (e.g. Lee and Horodyski, 2006; Mendes and Mirth, 2016), and wing development in ants (e.g.…”