Drive, suppression, and escape from suppression of a selfish chromosome

ABSTRACT Meiotic drivers are selfish chromosomes that are predicted to spark a rapid intragenomic arms-race with their suppressors. However, the long-term persistence of unsuppressed selfish chromosomes in natural populations violates these theoretical expectations. The Drosophila pseudoobscura Sex-Ratio ( SR ) chromosome exemplifies this problem, sometimes referred to as the “ancient gene drive paradox”. Here, we reconstruct the evolutionary history of this SR chromosome and show that its genetic architecture and complexity has been shaped by a history of drive, suppression, and escape from suppression. Our results indicate that the current lack of resistance to the SR chromosome represents a transient condition awaiting the emergence of new suppressors. SIGNIFICANCE Intragenomic arms races triggered by selfish chromosomes are expected to drive rapid evolution through cycles of drive, suppression, and escape from suppression. Despite these expectations, some selfish chromosomes such as the D. pseudoobscura Sex-Ratio ( SR ) chromosome exist unsuppressed for extended periods of time. Despite the absence of suppression, we uncover currently segregating suppressors against the ancestral version and evidence of recent dynamic evolution on the SR chromosome. Today’s SR chromosome thus represents a transient state in a surprisingly slow arms race. Taken together, the lack of suppressors against this selfish chromosome can be explained by mutational limits for the emergence of suppressors.