Cytoplasmic Male Sterility Declines in the Presence of Resistant Nuclear Backgrounds

AbstractGenomic conflicts arise when different genes in a genome are selected for opposite phenotypic effects. One well-known conflict occurs in plants, between mitochondrial genes causing cytoplasmic male sterility (CMS) and their nuclear suppressors, called restorers of male fertility. The evolution of CMS-restorer polymorphisms has been modeled many times, but empirical validations remain indirect. Here we use a new biological model, a freshwater snail, to directly observe evolutionary trajectories. In this species, CMS-associated mitogenomes coexist with male-fertile ones in populations. Models predict such a coexistence when nuclear restorers make CMS mitogenomes less fit than male-fertile ones, thus preventing the fixation of CMS. During 11 generations of experimental evolution, we observed rapid decreases in the frequency of CMS mitogenomes in a restorer-rich nuclear background, with an estimated ∼20% fitness disadvantage, consistent with theoretical conditions for the maintenance of cytonuclear polymorphism. In parallel, in an ancillary experiment, eggs laid by isolated snails carrying CMS showed a reduced hatching rate. Although significant, this reduction did not reach 20%, suggesting that fitness differentials in populations are enhanced by competition or rely on unmeasured traits. Our study illustrates the speed at which evolution can proceed in the context of cytonuclear conflicts over sex allocation.