Multiple recent sex chromosome fusions in Drosophila virilis associated with elevated satellite DNA abundance

Abstract

ABSTRACTRepetitive satellite DNA is highly variable both within and between species, and is often located near centromeres. However, the abundance or array length of satellite DNA may be constrained or have maximum limits. Drosophila virilis contains among the highest relative satellite abundances, with almost half its genome composed of three related 7 bp satellites. We discovered a strain of D. virilis that has 15% more pericentromeric satellite DNA compared to other strains, and also underwent two independent centromere-to-centromere sex chromosome fusion events. These fusions are presumably caused by DNA breakage near the pericentromeric satellites followed by repair using similar repetitive regions of nonhomologous chromosomes. We hypothesized that excess satellite DNA might increase the risk of DNA breaks and genome instability when stressed, which would be consistent with the apparent high rate of fusions we found in this strain. To directly quantify DNA breakage levels between strains with different satellite DNA abundances, we performed the comet assay after feeding flies gemcitabine and administering low-dose gamma radiation. We found a positive correlation between the rate of DNA breakage and satellite DNA abundance. This was further supported by a significant decrease in DNA breakage in an otherwise genetically identical substrain that lost the chromosome fusion and several megabases of satellite DNA. We find that the centromere-to-centromere fusions resulted in up to a 21% nondisjunction rate between the X and Y chromosomes in males, adding a fitness cost. Finally, we propose a model consistent with our data that implicates genome instability as a critical evolutionary constraint to satellite abundance.