Stress response, behavior, and development are shaped by transposable element-induced mutations in Drosophila

Most of the current knowledge on the genetic basis of adaptive evolution is based on the analysis of single nucleotide polymorphisms (SNPs). Despite increasing evidence for their causal role, the contribution of structural variants to adaptive evolution remains largely unexplored. In this work, we analyzed the population frequencies of 1,615 Transposable Element (TE) insertions annotated in the reference genome of Drosophila melanogaster, in 91 samples from 60 worldwide natural populations. We identified a set of 300 polymorphic TEs that are present at high population frequencies, and located in genomic regions with high recombination rate, where the efficiency of natural selection is high. The age and the length of these 300 TEs are consistent with relatively young and long insertions reaching high frequencies due to the action of positive selection. Besides, we identified a set of 21 fixed TEs also likely to be adaptive. Indeed, we, and others, found evidence of selection for 84 of these reference TE insertions. The analysis of the genes located nearby these 84 candidate adaptive insertions suggested that the functional response to selection is related with the GO categories of response to stimulus, behavior, and development. We further showed that a subset of the candidate adaptive TEs affects expression of nearby genes, and five of them have already been linked to an ecologically relevant phenotypic effect. Our results provide a more complete understanding of the genetic variation and the fitness-related traits relevant for adaptive evolution. Similar studies should help uncover the importance of TE-induced adaptive mutations in other species as well.Author summary: Transposable elements are fragments of genomic DNA that have the ability to move around the genome by creating new copies of themselves. Although there is evidence suggesting that transposable elements play important roles in genome function and genome evolution, our current understanding is based on the analysis of a subset of all transposable element insertions present in the genome, in only a few natural populations. Advances in genome sequencing and bioinformatics tools allow us now to investigate all transposable element insertions in genomes across continents. In this work, we analyzed the age, size, and frequency of 1,615 transposable elements in 91 samples from 60 worldwide natural populations of the model species Drosophila melanogaster. The genomic regions surrounding 84 transposable elements indicate that they could have an adaptive effect for the flies that carry them. These insertions are located nearby genes involved in stress response, behavior and development suggesting that these biological processes are affected by transposable element insertions.