Selection for mitonuclear co-adaptation could favour the evolution of two sexes

Mitochondria are descended from free-living bacteria that were engulfed by another cell between one and a half to two billion years ago. A redistribution of DNA led to most genetic information being lost or transferred to a large central genome in the nucleus, leaving a residual genome in each mitochondrion. Oxidative phosphorylation, the most critical function of mitochondria, depends on the functional compatibility of proteins encoded by both the nucleus and mitochondria. We investigate whether selection for adaptation between the nuclear and mitochondrial genomes (mitonuclear co-adaptation) could, in principle, have promoted uniparental inheritance of mitochondria and thereby the evolution of two mating types or sexes. Using a mathematical model, we explore the importance of the radical differences in ploidy levels, sexual and asexual modes of inheritance, and mutation rates of the nucleus and mitochondria. We show that the major features of mitochondrial inheritance, notably uniparental inheritance and bottlenecking, enhance the co-adaptation of mitochondrial and nuclear genes and therefore improve fitness. We conclude that, under a wide range of conditions, selection for mitonuclear co-adaptation favours the evolution of two distinct mating types or sexes in sexual species.