Rapid Evolution of Complete Dosage Compensation in Poecilia

Abstract

Dosage compensation balances gene expression between the sexes in systems with diverged heterogametic sex chromosomes. Theory predicts that dosage compensation should rapidly evolve in tandem with the divergence of sex chromosomes to prevent the deleterious effects of dosage imbalances that occur as a result of sex chromosome divergence. Examples of complete dosage compensation, where gene expression of the entire sex chromosome is compensated, are rare, and have only been found in relatively ancient sex chromosome systems. Consequently, very little is known about the evolutionary dynamics of complete dosage compensation systems. Within the family Poeciliidae the subgenus Lebistes share the same sex chromosome system which originated 18.48-26.08 Ma. In Poecilia reticulata and P. wingei, the Y chromosome has been largely maintained, whereas the Y in the closely related species P. picta and P. parae has rapidly degraded. We recently found P. picta to be the first example of complete dosage compensation in a fish. Here, we show that P. parae also has complete dosage compensation, thus complete dosage compensation likely evolved in the short (∼3.7 Myr) interval after the split of the ancestor of these two species from P. reticulata, but before they diverged from each other. These data suggest that novel dosage compensation mechanisms can evolve rapidly, thus supporting the longstanding theoretical prediction that such mechanisms arise in tandem with rapidly diverging sex chromosomes.