Exploring the phenotypic space of a putatively adaptive transposable element insertion in Drosophila

Abstract

The ínvader4 retro-transposon FBtí0019386 was identified as a putatively adaptive natural insertion in a genome-wide screening in Drosophíla melanogaster. In this study, we screened multiple phenotypes in several D. melanogaster natural populations differing by the presence/absence of this transposable element (TE) to identify the adaptive effect of this mutation. To do this, we took into account FBtí0019386 population frequency dynamics suggesting that it is involved in adaptation to temperate environments as well as the functional information available for the two closest genes. FBtí0019386 is inserted in the 5'UTR intron of sarah, a gene involved in a wide variety of processes such as ovulation, egg hatchability, fecundity or learning and memory. FBtí0019386 is located upstream of the 5'UTR of bicoid interacting protein 1 (Bin1), a negative regulator of transcription that plays a role in environmental stress response. We found that flies with and without the insertion do not differ in fecundity or egg hatchability. However, we observed that flies with the insertion are more sensitive to cold stress in adults, and slightly more sensitive to osmotic stress and starvation, while they do not differ in cold stress sensitivity in embryos. Our results also showed that flies with the insertion have a significantly shorter developmental time compared to flies without the insertion. The observed increased sensitivity to environmental stress is likely to be the cost of selection of this adaptive mutation, while a shorter developmental time is an adaptive fitness trait in nature that is associated with temperate environments adaptation. We also found that flies with FBtí0019386 insertion showed a down-regulation of sarah but not of Bin1 . This down-regulation is most probably dueto the introduction of piRNA-binding sites by FBti00193861eading to the recruitment of HP1 protein. While we cannot discard that other phenotypes such as fine-tuning regulation of learning and memory could also be affected by FBtí0019386, our results already show that TE-induced mutations have complex phenotypic effects with both positive and negative impacts on fitness.