Abstract
The uniparental inheritance (UPI) of mitochondria is thought to explain the evolution of two mating types or even true sexes with anisogametes. However, the exact role of UPI is not clearly understood. Here, we develop a new model, which considers the spread of UPI mutants within a biparental inheritance (BPI) population. Our model explicitly considers mitochondrial mutation and selection in parallel with the spread of UPI mutants and self-incompatible mating types. In line with earlier work, we find that UPI improves fitness under mitochondrial mutation accumulation, selfish conflict and mitonuclear coadaptation. However, we find that as UPI increases in the population its relative fitness advantage diminishes in a frequency-dependent manner. The fitness benefits of UPI ‘leak’ into the biparentally reproducing part of the population through successive matings, limiting the spread of UPI. Critically, while this process favours some degree of UPI, it neither leads to the establishment of linked mating types nor the collapse of multiple mating types to two. Only when two mating types exist beforehand can associated UPI mutants spread to fixation under the pressure of high mitochondrial mutation rate, large mitochondrial population size and selfish mutants. Variation in these parameters could account for the range of UPI actually observed in nature, from strict UPI in some Chlamydomonas species to BPI in yeast. We conclude that UPI of mitochondria alone is unlikely to have driven the evolution of two mating types in unicellular eukaryotes.
Highlights
The existence of two distinct sexes in the majority of sexual organisms poses a well-known conundrum in evolutionary biology [1]
A number of experimental and theoretical analyses indicate that Uniparental inheritance (UPI) of mitochondria can improve fitness and has led to the suggestion that this force underlies the evolution of two mating types, leading to anisogamy and the evolution of true sexes [8,9,10,11,12,13,14,26,27]
We show that the fitness benefits arising from UPI are acquired cumulatively, over multiple generations
Summary
The existence of two distinct sexes in the majority of sexual organisms poses a well-known conundrum in evolutionary biology [1]. The assumption of a fixed cost for BPI in these models is dubious, and needs to be further investigated as fitness reduction is expected to depend on the number of selfish mutations carried Such consideration was made in an earlier analysis by Hastings [13], who concluded that the spread of selfish mutants led to the evolution of UPI and anisogamy. Theoretical work again supports an advantage to UPI [14] and lacks formal consideration of the evolution transition from BPI to UPI These limitations and different models make it difficult to determine the conditions under which the fitness benefits of UPI are sufficient to drive the evolution of two distinct mating types in unicellular organisms. We discuss how our findings relate to previous analyses and to the patterns seen in protists
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