The emergence of a transcriptional silencer underlying the loss of a morphological trait

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Morphological diversity and the variation in discrete traits that composes it result, to a large extent, from changes in the regulation of developmental genes. Notably, variation in the regulatory sequences of these genes fuels evolutionary changes in gene expression. Transcriptional enhancers in particular respond to specific transcription factors and determine when, where and how much developmental genes are transcribed. The main focus in the evolutionary literature to explain the variation of enhancer activities is the turnover of binding sites for these transcription factors. It was recently suggested, however, that the accessibility of enhancer sequences, determined by the degree of chromatin compaction, may also explain the variation of enhancer activities and thereby modulate gene expression. Yet, this regulatory level, chromatin accessibility, has not been examined from this evolutionary standpoint. The present proposal attempts to bridge this gap by studying the role of chromatin accessibility in the evolution of a discrete morphological character, a pigmentation spot at the tip of the wing in flies (Drosophila). Namely, we have identify intriguing changes in the accessibility in the regulatory regions of the pigmentation gene yellow, between a spotted species and a species that has secondarily lost its spot. Yellow expression underlies the formation of the spot, and variation in its expression represent an important evolutionary node explaining wing pigmentation diversity. Combining reporter assays in transgenic Drosophila and genomic profiling (ATAC-seq, ChiP-seq) of these regions, we will decipher by which molecular mechanisms changes of chromatin accessibility may have modulated the expression of a gene during an evolutionary transition.