Evolution of mating types driven by purifying selection against mitochondrial mutations

Abstract

Sexual cell fusion combines genetic material of two gametes, but why the two reproductive cells have to belong to distinct self-incompatible gamete classes is not known. In a vast majority of sexual eukaryotes, mitochondria are inherited uniparentally from only one of the two mating types, which is thought to facilitate purifying selection against deleterious mitochondrial mutations and limit the inter-genomic conflicts. Here I argue that two mating types in eukaryotes represent a mechanism of mitochondrial quality control through the highly asymmetric transmission of mitochondrial genes at cell fusion. I develop a mathematical model to explicitly study the evolution of two self-incompatible mating type alleles linked to the nuclear locus controlling the pattern of organelle inheritance. The invasion of mating-type alleles is opposed by the short-term fitness benefit of mitochondrial mixing under negative epistasis and the lower chance of encountering a compatible mating partner. Nevertheless, under high mitochondrial mutation rates purifying selection against defective mitochondria can drive two mating types with uniparental inheritance to fixation. The invasion is further facilitated by the paternal leakage of mitochondria under paternal control of cytoplasmic inheritance. In contrast to previous studies, the model does not rely on the presence of selfish cytoplasmic elements, providing a more universal solution to the longstanding evolutionary puzzle of two sexes.