Selection against heteroplasmy explains the evolution of uniparental inheritance of mitochondria

Why are mitochondria almost always inherited from one parent during sexual reproduction? Current explanations for this evolutionary mystery include conflict avoidance between the nuclear and mitochondrial genomes, clearing of deleterious mutations, and optimization of mitochondrial-nuclear coadaptat...

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Bibliographic Details
Published in:PLoS genetics 2015-04, Vol.11 (4), p.e1005112-e1005112
Main Authors: Christie, Joshua R, Schaerf, Timothy M, Beekman, Madeleine
Format: Article
Language:English
Subjects:
Algae
Animals
Charitable foundations
Divisions
Epigenetic inheritance
Equilibrium
Evolution
Evolution, Molecular
Genes, Mitochondrial
Genomes
Haplotypes
Humans
Hypotheses
Identification and classification
Mathematical models
Mitochondria
Mitochondria - genetics
Models, Genetic
Mutation
Phosphorylation
Physiological aspects
Selection, Genetic
Theory
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Summary:Why are mitochondria almost always inherited from one parent during sexual reproduction? Current explanations for this evolutionary mystery include conflict avoidance between the nuclear and mitochondrial genomes, clearing of deleterious mutations, and optimization of mitochondrial-nuclear coadaptation. Mathematical models, however, fail to show that uniparental inheritance can replace biparental inheritance under any existing hypothesis. Recent empirical evidence indicates that mixing two different but normal mitochondrial haplotypes within a cell (heteroplasmy) can cause cell and organism dysfunction. Using a mathematical model, we test if selection against heteroplasmy can lead to the evolution of uniparental inheritance. When we assume selection against heteroplasmy and mutations are neither advantageous nor deleterious (neutral mutations), uniparental inheritance replaces biparental inheritance for all tested parameter values. When heteroplasmy involves mutations that are advantageous or deleterious (non-neutral mutations), uniparental inheritance can still replace biparental inheritance. We show that uniparental inheritance can evolve with or without pre-existing mating types. Finally, we show that selection against heteroplasmy can explain why some organisms deviate from strict uniparental inheritance. Thus, we suggest that selection against heteroplasmy explains the evolution of uniparental inheritance.
ISSN:1553-7404
1553-7390
1553-7404
DOI:10.1371/journal.pgen.1005112