Phenotypic Plasticity through Transcriptional Regulation of the Evolutionary Hotspot Gene tan in Drosophila melanogaster

Abstract

Phenotypic plasticity is the ability of a given genotype to produce different phenotypes in response to distinct environmental conditions. Phenotypic plasticity can be adaptive. Furthermore, it is thought to facilitate evolution. Although phenotypic plasticity is a widespread phenomenon, its molecular mechanisms are only beginning to be unravelled. Environmental conditions can affect gene expression through modification of chromatin structure, mainly via histone modifications, nucleosome remodelling or DNA methylation, suggesting that phenotypic plasticity might partly be due to chromatin plasticity. As a model of phenotypic plasticity, we study abdominal pigmentation of Drosophila melanogaster females, which is temperature sensitive. Abdominal pigmentation is indeed darker in females grown at 18°C than at 29°C. This phenomenon is thought to be adaptive as the dark pigmentation produced at lower temperature increases body temperature. We show here that temperature modulates the expression of tan (t), a pigmentation gene involved in melanin production. t is expressed 7 times more at 18°C than at 29°C in female abdominal epidermis. Genetic experiments show that modulation of t expression by temperature is essential for female abdominal pigmentation plasticity. Temperature modulates the activity of an enhancer of t without modifying compaction of its chromatin or level of the active histone mark H3K27ac. By contrast, the active mark H3K4me3 on the t promoter is strongly modulated by temperature. The H3K4 methyl-transferase involved in this process is likely Trithorax, as we show that it regulates t expression and the H3K4me3 level on the t promoter and also participates in female pigmentation and its plasticity. Interestingly, t was previously shown to be involved in inter-individual variation of female abdominal pigmentation in Drosophila melanogaster, and in abdominal pigmentation divergence between Drosophila species. Sensitivity of t expression to environmental conditions might therefore give more substrate for selection, explaining why this gene has frequently been involved in evolution of pigmentation.

Using Drosophila pigmentation traits to study the mechanisms of cis-regulatory evolution

“…With the growing recognition that phenomena such as developmental plasticity, constraint, and robustness can play important evolutionary roles [38,39], traits like fruit fly pigmentation [40,41], for which the molecular basis of their construction and evolution have been worked out to the finest resolution will lead the way in providing concrete details of how these processes work mechanistically. Indeed, pigmentation of the female D. melanogaster posterior abdomen is influenced by temperature, and both bab [41] and tan [42] have been implicated in the environmental response. An understanding of these genes’ CRE regulatory logic should allow insights to be made about the role of transcriptional regulatory sequences in the evolution of plasticity.…”

A Variable Genetic Architecture of Melanic Evolution inDrosophila melanogaster

“…This SNP is tightly linked to a short indel 7-bp away. Nearby sequence closer to the promoter was recently shown to underlie thermal plasticity in pigmentation (Gibert et al 2016). …”

Pleiotropic effects of regulatory variation in tan result in correlation of two pigmentation traits in Drosophila melanogaster

“…The ebony regulatory sequences regulating its expression in the trident overlap with the activator element (Rebeiz et al., ). For tan , the tMSE element drives GFP expression in abdominal epidermis in males (Jeong et al., ) and females (Gibert et al., ) as well as in the trident (Gibert et al., ). This explains how SNPs located in this enhancer can affect both female abdominal pigmentation and the trident.…”

“…Plasticity of abdominal pigmentation has been linked to expression levels of tan , with the tMSE playing a prominent role. Other enzymes, such as yellow , are only contributing to a lesser extent (Gibert, Mouchel‐Vielh, De Castro, & Peronnet, ; Gibert, Mouchel‐Vielh, & Peronnet, ). In contrast to abdominal pigmentation, the regulation of the trident is less understood.…”

“…Other enzymes, such as yellow, are only contributing to a lesser extent (Gibert, Mouchel-Vielh, De Castro, & Peronnet, 2016;Gibert, Mouchel-Vielh, & Peronnet, 2017). In contrast to abdominal pigmentation, the regulation of the trident is less understood.…”