The genetic basis of trichome loss in D. sechellia

Morphology evolves predominantly by changes in gene regulation due to mutations in developmental enhancers. However, only few studies have identified the causal mutations in evolved enhancers that contributed to morphological differences between species. Here we address these issues by studying evolved enhancers of the Drosophila shavenbaby gene.

Shavenbaby encodes a transcription factor that controls the development of cuticular hair-like projections called trichomes. Trichome patterns have repeatedly evolved in larvae of the genus Drosophila through changes in the shavenbaby regulatory regions. Seven enhancers, located in the cis-regulatory region of shavenbaby, control its complex embryonic expression. In D. sechellia, a sister species to D. melanogaster, five of these enhancers have evolved reduced embryonic activity, leading to the evolution of naked larvae. We have previously identified the causal mutations and revealed the complete molecular mechanisms underlying the loss of one of these enhancers, named E6, in D. sechellia, but the genetic basis underlying the loss of function of the other enhancers remains unknown.

Here, we use reporter gene assays to identify the causal mutations that altered the function of all the D. sechellia shavenbaby enhancers. We find that, like the D. sechellia E6 enhancer, two additional D. sechellia shavenbaby enhancers have evolved through gain of repression. In contrast, the D. sechellia shavenbaby Z1.3 enhancer accumulated a 120-nucleotide deletion in the core enhancer that eliminated most of its embryonic activity. Our future studies will reveal how many and what type of cis-regulatory changes underly a simple evolutionary transition such as the loss of trichomes.