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.

Rapid evolution of a Y-chromosome heterochromatin protein underlies sex chromosome meiotic drive

“…The first locus colocalizes with the tandem duplication of a 37-kb segment spanning six genes [hereafter duplication SR (Dp SR )]. The second locus (Wlasta) was mapped about 110 kb away from Dp SR within a 42-kb interval showing no large rearrangements (13,14). Here, we show that Wlasta is heterochromatin protein 1 D2 (HP1D2), a young member of the HP1 gene family, and we characterize HP1D2 alleles that cause the drive.…”

“…According to the estimated age of Dp SR (<500 y) (14), the spread of the Paris drivers is recent, and their evolution in populations is very fast (20,21). Through its own spreading, together with Dp SR , the HP1D2 SR allele carried by X SR4 (lacking CSD) became the most frequent allele in the Malagasy populations (based on the selective sweep studied in refs.…”

Meiotic drive mechanisms: lessons fromDrosophila

“…The first implication of a heterochromatin protein in meiotic drive was in the D. simulans Paris SR system where the distortion results from an interaction between two X-linked drive loci. The first drive locus maps to a 37 kb tandem duplication containing six genes; however, the molecular identity of the causal element within this duplication is still unknown [7,34]. The second driver corresponds to HP1D2 [17], a young and rapidly evolving member of the HP1 (heterochromatin protein Figure 1.…”

Local dynamics of a fast‐evolving sex‐ratio system in Drosophila simulans

“…): one of them is a segmental duplication of six genes that would have arisen <500 years ago (Fouvry et al . ), whereas the other locus is still not identified but lies between the Nrg and Crag genes (a region including 11 candidate genes, see Fig. ).…”