Ancient gene drives: an evolutionary paradox

Abstract

Selfish genetic elements such as selfish chromosomes increase their transmission rate relative to the rest of the genome and can generate substantial cost to the organisms that carry them. Such segregation distorters are predicted to either reach fixation (potentially causing population extinction) or, more commonly, promote the evolution of genetic suppression to restore transmission to equality. Many populations show rapid spread of segregation distorters, followed by the rapid evolution of suppression. However, not all drivers display such flux, some instead persisting at stable frequencies in natural populations for decades, perhaps hundreds of thousands of years, with no sign of suppression evolving or the driver spreading to fixation. This represents a major evolutionary paradox. How can drivers be maintained in the long term at stable frequencies? And why has suppression not evolved as in many other gene drive systems? Here, we explore potential factors that may explain the persistence of drive systems, focusing on the ancient sex-ratio driver in the fly Drosophila pseudoobscura. We discuss potential solutions to the evolutionary mystery of why suppression does not appear to have evolved in this system, and address how long-term stable frequencies of gene drive can be maintained. Finally, we speculate whether ancient drivers may be functionally and evolutionarily distinct to young drive systems.