Sequence Analysis of the Segmental Duplication Responsible for ParisSex-RatioDrive inDrosophila simulans

Abstract

Sex-ratio distorters are X-linked selfish genetic elements that facilitate their own transmission by subverting Mendelian segregation at the expense of the Y chromosome. Naturally occurring cases of sex-linked distorters have been reported in a variety of organisms, including several species of Drosophila; they trigger genetic conflict over the sex ratio, which is an important evolutionary force. However, with a few exceptions, the causal loci are unknown. Here, we molecularly characterize the segmental duplication involved in the Paris sex-ratio system that is still evolving in natural populations of Drosophila simulans. This 37.5 kb tandem duplication spans six genes, from the second intron of the Trf2 gene (TATA box binding protein-related factor 2) to the first intron of the org-1 gene (optomotor-blind-related-gene-1). Sequence analysis showed that the duplication arose through the production of an exact copy on the template chromosome itself. We estimated this event to be less than 500 years old. We also detected specific signatures of the duplication mechanism; these support the Duplication-Dependent Strand Annealing model. The region at the junction between the two duplicated segments contains several copies of an active transposable element, Hosim1, alternating with 687 bp repeats that are noncoding but transcribed. The almost-complete sequence identity between copies made it impossible to complete the sequencing and assembly of this region. These results form the basis for the functional dissection of Paris sex-ratio drive and will be valuable for future studies designed to better understand the dynamics and the evolutionary significance of sex chromosome drive.