Adaptive co-evolution of mitochondria and the Y-chromosome: A resolution to conflict between evolutionary opponents

Abstract

In most species with motile sperm, male fertility depends upon genes located on the Y-chromosome and in the mitochondrial genome. Coordinated adaptive evolution for the function of male fertility between genes on the Y and the mitochondrion is hampered by their uniparental inheritance in opposing sexes: The Y-chromosome is inherited uniparentally, father to son, and the mitochondrion is inherited maternally, mother to offspring. Preserving male fertility is problematic, because maternal inheritance permits mitochondrial mutations advantageous to females, but deleterious to male fertility, to accumulate in a population. Although uniparental inheritance with sex-restricted adaptation also affects genes on the Y-chromosome, females lack a Y-chromosome and escape the potential maladaptive consequences of male-limited selection. Evolutionary models have shown that mitochondrial mutations deleterious to male fertility can be countered by compensatory evolution of Y-linked mutations that restore it. However, direct adaptive coevolution of Y- and mitochondrial gene combinations has not yet been mathematically characterized. We use population genetic models to show that adaptive coevolution of Y and mitochondrial genes are possible when Y-mt gene combinations have positive effects on male fertility and populations are inbred.