Long-term Persistence of an Unsuppressed Selfish Chromosome

Many species harbor selfish chromosomes that trigger the evolution of resistant target chromosomes or other suppressors. However, the existence of unsuppressed selfish chromosomes in natural populations challenges evolutionary theory. Here, we report the reconstruction of the evolutionary history of the Drosophila pseudoobscura Sex-Ratio chromosome, which exemplifies the ancient gene drive paradox - the long-term maintenance of unsuppressed selfish chromosomes. We show that although today there is no resistance to, or suppression of, this Sex-Ratio chromosome, its genetic architecture and complexity has been shaped by a history of distortion, suppression, and escape from suppression. This history provides the first definitive example of intra-genomic conflicts fueling an evolutionary arms race. The lack of suppression of the D. pseudoobscura Sex-Ratio chromosome today suggests that the speed of evolutionary arms races may slow down as drive systems become more complex over time and raises the possibility that the immediate emergence of resistance to some gene drive systems is not inevitable. Thus, strong, persistent, long-term selection imposed by gene-drive systems may not be sufficient to drive the evolution of suppression of the driver.