Transcriptional polymorphism of piRNA regulatory genes underlies the mariner activity in Drosophila simulans testes.

During colonization of new areas, natural populations have to deal with changing environments, and transposable elements (TEs) can be useful "tools" in the adaptation process as they are major contributor to the structural and functional evolution of genomes. In this general context, the activity (copy number, transcriptional and excision rate) of the mariner mos1 element was estimated in 19 natural populations of D. simulans. It is shown (i) that mos1 expression is always higher and more variable in testes than in ovaries; (ii) that mos1 activity is higher in colonizing populations compared to the sub-Saharan African ones (ancestral populations); (iii) that mos1 variations in transcript levels and copy number are negatively correlated with transcriptional variations of piRNA genes, aubergine and argonaute3. Furthermore, mos1 levels of expression in testes highly contrast with the low expression patterns of ago3. These results strongly suggest that the expression polymorphism of piRNA genes could be responsible for the mos1 variations, first between male and female germlines and second, according to the status of natural populations (colonizing or not). These results provide new perspectives about TEs and piRNA genes co-evolution in Drosophila germlines.