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Selection against heteroplasmy explains the evolution of uniparental inheritance of mitochondria.

Christie JR, Schaerf TM, Beekman M - PLoS Genet. (2015)

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: School of Biological Sciences, The University of Sydney, Sydney, Australia; Centre for Mathematical Biology, The University of Sydney, Sydney, Australia.

ABSTRACT
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.

No MeSH data available.


Fitness and distribution of cell types.Parameters: n = 20, μ = 10−4, ch = 0.2 and concave fitness. U1B2 cells appear at generation 0, which is the point at which the B1 and B2 gametes reach mutation-selection equilibrium. (A) Relative advantage of each genotype through time (see Model for details). For B-E, the relative proportion is the sum of a particular cell type divided by the sum of all cells that carry the same genotype. The heteroplasmic category includes all cells with any level of heteroplasmy. B-C shows the distribution of cells carrying the U1B2 genotype (B) and the B1B2 genotype (C). D-E show a more detailed distribution of cell types carrying the B1B2 genotype at generation 1350 (D) and at generation 1820 (E). The decrease in heteroplasmy in B1B2 cells between generations 0–100 is an artifact of introducing U1 at a frequency of 0.01 (the influx of U1 gametes homoplasmic for the wild type haplotype converts some heteroplasmic B1 and B2 gametes into homoplasmic gametes, which increases the proportion of homoplasmic B1B2 cells). From generations 1350–1820, the proportion of heteroplasmic B1B2 cells decreases (C) but the level of heteroplasmy increases (compare D with E). This more than offsets the decrease in the proportion of heteroplasmic cells and  continues to decrease (A).
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pgen.1005112.g002: Fitness and distribution of cell types.Parameters: n = 20, μ = 10−4, ch = 0.2 and concave fitness. U1B2 cells appear at generation 0, which is the point at which the B1 and B2 gametes reach mutation-selection equilibrium. (A) Relative advantage of each genotype through time (see Model for details). For B-E, the relative proportion is the sum of a particular cell type divided by the sum of all cells that carry the same genotype. The heteroplasmic category includes all cells with any level of heteroplasmy. B-C shows the distribution of cells carrying the U1B2 genotype (B) and the B1B2 genotype (C). D-E show a more detailed distribution of cell types carrying the B1B2 genotype at generation 1350 (D) and at generation 1820 (E). The decrease in heteroplasmy in B1B2 cells between generations 0–100 is an artifact of introducing U1 at a frequency of 0.01 (the influx of U1 gametes homoplasmic for the wild type haplotype converts some heteroplasmic B1 and B2 gametes into homoplasmic gametes, which increases the proportion of homoplasmic B1B2 cells). From generations 1350–1820, the proportion of heteroplasmic B1B2 cells decreases (C) but the level of heteroplasmy increases (compare D with E). This more than offsets the decrease in the proportion of heteroplasmic cells and continues to decrease (A).

Mentions: In our model, heteroplasmic cells are generated by mutation. During meiosis, heteroplasmic cells produce gametes with varying levels of heteroplasmy, including homoplasmic gametes. Uniparental inheritance maintains this variation created by meiosis, which leads to homoplasmic U1B2 cells (Fig 2A–2B and S2A–S2B Fig). Mutants that arise in U1B2 cells quickly segregate into U1 gametes that carry mutant haplotypes only (Fig 3A–3B and S3A–S3B Fig), which leads to U1B2 cells that are homoplasmic for mutant mitochondria (Fig 2B and S2B Fig). Since we assume that mutations are neutral, cells homoplasmic for mutant mitochondria suffer no fitness costs.


Selection against heteroplasmy explains the evolution of uniparental inheritance of mitochondria.

Christie JR, Schaerf TM, Beekman M - PLoS Genet. (2015)

Fitness and distribution of cell types.Parameters: n = 20, μ = 10−4, ch = 0.2 and concave fitness. U1B2 cells appear at generation 0, which is the point at which the B1 and B2 gametes reach mutation-selection equilibrium. (A) Relative advantage of each genotype through time (see Model for details). For B-E, the relative proportion is the sum of a particular cell type divided by the sum of all cells that carry the same genotype. The heteroplasmic category includes all cells with any level of heteroplasmy. B-C shows the distribution of cells carrying the U1B2 genotype (B) and the B1B2 genotype (C). D-E show a more detailed distribution of cell types carrying the B1B2 genotype at generation 1350 (D) and at generation 1820 (E). The decrease in heteroplasmy in B1B2 cells between generations 0–100 is an artifact of introducing U1 at a frequency of 0.01 (the influx of U1 gametes homoplasmic for the wild type haplotype converts some heteroplasmic B1 and B2 gametes into homoplasmic gametes, which increases the proportion of homoplasmic B1B2 cells). From generations 1350–1820, the proportion of heteroplasmic B1B2 cells decreases (C) but the level of heteroplasmy increases (compare D with E). This more than offsets the decrease in the proportion of heteroplasmic cells and  continues to decrease (A).
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pgen.1005112.g002: Fitness and distribution of cell types.Parameters: n = 20, μ = 10−4, ch = 0.2 and concave fitness. U1B2 cells appear at generation 0, which is the point at which the B1 and B2 gametes reach mutation-selection equilibrium. (A) Relative advantage of each genotype through time (see Model for details). For B-E, the relative proportion is the sum of a particular cell type divided by the sum of all cells that carry the same genotype. The heteroplasmic category includes all cells with any level of heteroplasmy. B-C shows the distribution of cells carrying the U1B2 genotype (B) and the B1B2 genotype (C). D-E show a more detailed distribution of cell types carrying the B1B2 genotype at generation 1350 (D) and at generation 1820 (E). The decrease in heteroplasmy in B1B2 cells between generations 0–100 is an artifact of introducing U1 at a frequency of 0.01 (the influx of U1 gametes homoplasmic for the wild type haplotype converts some heteroplasmic B1 and B2 gametes into homoplasmic gametes, which increases the proportion of homoplasmic B1B2 cells). From generations 1350–1820, the proportion of heteroplasmic B1B2 cells decreases (C) but the level of heteroplasmy increases (compare D with E). This more than offsets the decrease in the proportion of heteroplasmic cells and continues to decrease (A).
Mentions: In our model, heteroplasmic cells are generated by mutation. During meiosis, heteroplasmic cells produce gametes with varying levels of heteroplasmy, including homoplasmic gametes. Uniparental inheritance maintains this variation created by meiosis, which leads to homoplasmic U1B2 cells (Fig 2A–2B and S2A–S2B Fig). Mutants that arise in U1B2 cells quickly segregate into U1 gametes that carry mutant haplotypes only (Fig 3A–3B and S3A–S3B Fig), which leads to U1B2 cells that are homoplasmic for mutant mitochondria (Fig 2B and S2B Fig). Since we assume that mutations are neutral, cells homoplasmic for mutant mitochondria suffer no fitness costs.

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: School of Biological Sciences, The University of Sydney, Sydney, Australia; Centre for Mathematical Biology, The University of Sydney, Sydney, Australia.

ABSTRACT
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.

No MeSH data available.