Abstract
BackgroundMitochondria are predominantly inherited from the maternal gamete, even in unicellular organisms. Yet an extraordinary array of mechanisms enforce uniparental inheritance, which implies shifting selection pressures and multiple origins.ResultsWe consider how this high turnover in mechanisms controlling uniparental inheritance arises using a novel evolutionary model in which control of mitochondrial transmission occurs either during spermatogenesis (by paternal nuclear genes) or at/after fertilization (by maternal nuclear genes). The model treats paternal leakage as an evolvable trait. Our evolutionary analysis shows that maternal control consistently favours strict uniparental inheritance with complete exclusion of sperm mitochondria, whereas some degree of paternal leakage of mitochondria is an expected outcome under paternal control. This difference arises because mito-nuclear linkage builds up with maternal control, allowing the greater variance created by asymmetric inheritance to boost the efficiency of purifying selection and bring benefits in the long term. In contrast, under paternal control, mito-nuclear linkage tends to be much weaker, giving greater advantage to the mixing of cytotypes, which improves mean fitness in the short term, even though it imposes a fitness cost to both mating types in the long term.ConclusionsSexual conflict is an inevitable outcome when there is competition between maternal and paternal control of mitochondrial inheritance. If evolution has led to complete uniparental inheritance through maternal control, it creates selective pressure on the paternal nucleus in favour of subversion through paternal leakage, and vice versa. This selective divergence provides a reason for the repeated evolution of novel mechanisms that regulate the transmission of paternal mitochondria, both in the fertilized egg and spermatogenesis. Our analysis suggests that the widespread occurrence of paternal leakage and prevalence of heteroplasmy are natural outcomes of this sexual conflict.
Highlights
Mitochondria are predominantly inherited from the maternal gamete, even in unicellular organisms
Under “paternal” control, nuclear genes in one mating type destroy their own mitochondria during gametogenesis, which is equivalent to the exclusion or disabling of mitochondria during spermatogenesis in multicellular organisms
Mathematical model We develop a mathematical model representing an infinite population of unicellular sexual haploid individuals, containing M mitochondria each
Summary
Mitochondria are predominantly inherited from the maternal gamete, even in unicellular organisms. Under “paternal” control, nuclear genes in one mating type destroy their own mitochondria during gametogenesis, which is equivalent to the exclusion or disabling of mitochondria during spermatogenesis (before entering the oocyte) in multicellular organisms. Under these definitions, the mating type that contributes the greater number of mitochondria to the generation is maternal, and the mating type contributing less is paternal. The conclusion holds true for multicellular organisms with anisogamy, as the same problem remains — a paternal nuclear gene that causes the exclusion of sperm mitochondria cannot build up linkage with maternally inherited organelles, as this relationship is re-set every generation
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