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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.


Recombination and no mating types scenarios.Parameters: n = 20, μ = 10−4, ch = 0.2. (A) As the U allele initially spreads (generations 0–1700), the U1B2/U2B1 genotypes increase in frequency. But, because U1B2 and U2B1 cells lead to B1B2 cells through meiosis and random mating, the U1U2 genotype soon takes over and uniparental inheritance becomes fixed. Additional parameters: Pr = 0.5 and concave fitness. (B) Biparental inheritance dominates when U × U matings are biparental and fitness is concave. (C) Uniparental inheritance invades to its maximum value (0.5) when U × U matings are biparental and fitness is linear or convex. (The frequency of uniparental inheritance is the sum of U1U2 and U2B1.) Additional parameters: linear fitness. (D)U × U matings have a mixture of uniparental and biparental inheritance. Unlike in B, U1U2 no longer becomes fixed because some U × U matings now have biparental inheritance and further increasing U1U2 would only increase the overall level of biparental inheritance. Additional parameters: Pb = 0.1 and linear fitness. (E) Lines represent the frequency of uniparental inheritance in separate simulations with linear fitness and varying probabilities of biparental inheritance (Pb) when U × U matings have a mixture of uniparental and biparental inheritance. As Pb increases, U × U matings are more likely to lead to biparental inheritance, which decreases the frequency of uniparental inheritance at equilibrium. (F) No mating types scenario under concave fitness. F is identical to A except that the frequency of UB in F is the sum of the U1B2 and U2B1 freqencies in A.
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pgen.1005112.g004: Recombination and no mating types scenarios.Parameters: n = 20, μ = 10−4, ch = 0.2. (A) As the U allele initially spreads (generations 0–1700), the U1B2/U2B1 genotypes increase in frequency. But, because U1B2 and U2B1 cells lead to B1B2 cells through meiosis and random mating, the U1U2 genotype soon takes over and uniparental inheritance becomes fixed. Additional parameters: Pr = 0.5 and concave fitness. (B) Biparental inheritance dominates when U × U matings are biparental and fitness is concave. (C) Uniparental inheritance invades to its maximum value (0.5) when U × U matings are biparental and fitness is linear or convex. (The frequency of uniparental inheritance is the sum of U1U2 and U2B1.) Additional parameters: linear fitness. (D)U × U matings have a mixture of uniparental and biparental inheritance. Unlike in B, U1U2 no longer becomes fixed because some U × U matings now have biparental inheritance and further increasing U1U2 would only increase the overall level of biparental inheritance. Additional parameters: Pb = 0.1 and linear fitness. (E) Lines represent the frequency of uniparental inheritance in separate simulations with linear fitness and varying probabilities of biparental inheritance (Pb) when U × U matings have a mixture of uniparental and biparental inheritance. As Pb increases, U × U matings are more likely to lead to biparental inheritance, which decreases the frequency of uniparental inheritance at equilibrium. (F) No mating types scenario under concave fitness. F is identical to A except that the frequency of UB in F is the sum of the U1B2 and U2B1 freqencies in A.

Mentions: When U1 × U2 matings lead to uniparental inheritance, the U1U2 genotype always spreads until it is fixed in the population, leading to complete uniparental inheritance (Fig 4A and S16–S18 Tables). When U1 × U2 matings lead to biparental inheritance, however, uniparental inheritance does not become fixed and the population reaches a polymorphic equilibrium (Fig 4B–4C). Under these conditions, the frequency of uniparental inheritance at equilibrium is ≤ 0.5 (S19–S21 Tables). Uniparental inheritance cannot exceed 0.5 because increasing the frequency of U1 or U2 simply increases the proportion of biparental U1 × U2 matings. The frequency of uniparental inheritance remains very low when we assume a concave fitness function (Fig 4B), but reaches its maximum (0.5) when we assume a linear or convex fitness function (Fig 4C) (see S12–S13 Figs. for an explanation).


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

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

Recombination and no mating types scenarios.Parameters: n = 20, μ = 10−4, ch = 0.2. (A) As the U allele initially spreads (generations 0–1700), the U1B2/U2B1 genotypes increase in frequency. But, because U1B2 and U2B1 cells lead to B1B2 cells through meiosis and random mating, the U1U2 genotype soon takes over and uniparental inheritance becomes fixed. Additional parameters: Pr = 0.5 and concave fitness. (B) Biparental inheritance dominates when U × U matings are biparental and fitness is concave. (C) Uniparental inheritance invades to its maximum value (0.5) when U × U matings are biparental and fitness is linear or convex. (The frequency of uniparental inheritance is the sum of U1U2 and U2B1.) Additional parameters: linear fitness. (D)U × U matings have a mixture of uniparental and biparental inheritance. Unlike in B, U1U2 no longer becomes fixed because some U × U matings now have biparental inheritance and further increasing U1U2 would only increase the overall level of biparental inheritance. Additional parameters: Pb = 0.1 and linear fitness. (E) Lines represent the frequency of uniparental inheritance in separate simulations with linear fitness and varying probabilities of biparental inheritance (Pb) when U × U matings have a mixture of uniparental and biparental inheritance. As Pb increases, U × U matings are more likely to lead to biparental inheritance, which decreases the frequency of uniparental inheritance at equilibrium. (F) No mating types scenario under concave fitness. F is identical to A except that the frequency of UB in F is the sum of the U1B2 and U2B1 freqencies in A.
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Related In: Results  -  Collection

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pgen.1005112.g004: Recombination and no mating types scenarios.Parameters: n = 20, μ = 10−4, ch = 0.2. (A) As the U allele initially spreads (generations 0–1700), the U1B2/U2B1 genotypes increase in frequency. But, because U1B2 and U2B1 cells lead to B1B2 cells through meiosis and random mating, the U1U2 genotype soon takes over and uniparental inheritance becomes fixed. Additional parameters: Pr = 0.5 and concave fitness. (B) Biparental inheritance dominates when U × U matings are biparental and fitness is concave. (C) Uniparental inheritance invades to its maximum value (0.5) when U × U matings are biparental and fitness is linear or convex. (The frequency of uniparental inheritance is the sum of U1U2 and U2B1.) Additional parameters: linear fitness. (D)U × U matings have a mixture of uniparental and biparental inheritance. Unlike in B, U1U2 no longer becomes fixed because some U × U matings now have biparental inheritance and further increasing U1U2 would only increase the overall level of biparental inheritance. Additional parameters: Pb = 0.1 and linear fitness. (E) Lines represent the frequency of uniparental inheritance in separate simulations with linear fitness and varying probabilities of biparental inheritance (Pb) when U × U matings have a mixture of uniparental and biparental inheritance. As Pb increases, U × U matings are more likely to lead to biparental inheritance, which decreases the frequency of uniparental inheritance at equilibrium. (F) No mating types scenario under concave fitness. F is identical to A except that the frequency of UB in F is the sum of the U1B2 and U2B1 freqencies in A.
Mentions: When U1 × U2 matings lead to uniparental inheritance, the U1U2 genotype always spreads until it is fixed in the population, leading to complete uniparental inheritance (Fig 4A and S16–S18 Tables). When U1 × U2 matings lead to biparental inheritance, however, uniparental inheritance does not become fixed and the population reaches a polymorphic equilibrium (Fig 4B–4C). Under these conditions, the frequency of uniparental inheritance at equilibrium is ≤ 0.5 (S19–S21 Tables). Uniparental inheritance cannot exceed 0.5 because increasing the frequency of U1 or U2 simply increases the proportion of biparental U1 × U2 matings. The frequency of uniparental inheritance remains very low when we assume a concave fitness function (Fig 4B), but reaches its maximum (0.5) when we assume a linear or convex fitness function (Fig 4C) (see S12–S13 Figs. for an explanation).

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.