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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 gamete types.Parameters: n = 20, μ = 10−4, ch = 0.2 and concave fitness. U1 gametes appear at generation 0, which is the point at which the B1 and B2 gametes reach mutation-selection equilibrium. (A) Relative advantage of each gamete through time (see Model for details). For B-F, the relative proportion is the sum of a particular gamete type (e.g. a homoplasmic wild type U1 gamete) divided by the sum of all cells carrying that allele (all gametes carrying the U1 allele). Thus, the relative proportion describes how an allele is distributed across different gamete types but it does not show their actual frequencies in the population. The heteroplasmic category combines all gametes with any level of heteroplasmy. B-D show the distribution of gametes carrying the U1 allele (B), B1 allele (C) and the B2 allele (D). E-F show a more detailed distribution of gametes carrying the B1 allele at generation 1350 (E) and generation 1820 (F). The decrease in heteroplasmy in B1 and B2 gametes 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). From generations 1350–1820, the proportion of heteroplasmic B1 and B2 gametes decreases (C and D) but the level of heteroplasmy increases (compare E with F). This more than offsets the decrease in the proportion of heteroplasmic cells and  continues to decrease (A). Around generation 1350, B2 gametes homoplasmic for mutant mitochondria begin to appear, which causes  to increase and eventually converge with .
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pgen.1005112.g003: Fitness and distribution of gamete types.Parameters: n = 20, μ = 10−4, ch = 0.2 and concave fitness. U1 gametes appear at generation 0, which is the point at which the B1 and B2 gametes reach mutation-selection equilibrium. (A) Relative advantage of each gamete through time (see Model for details). For B-F, the relative proportion is the sum of a particular gamete type (e.g. a homoplasmic wild type U1 gamete) divided by the sum of all cells carrying that allele (all gametes carrying the U1 allele). Thus, the relative proportion describes how an allele is distributed across different gamete types but it does not show their actual frequencies in the population. The heteroplasmic category combines all gametes with any level of heteroplasmy. B-D show the distribution of gametes carrying the U1 allele (B), B1 allele (C) and the B2 allele (D). E-F show a more detailed distribution of gametes carrying the B1 allele at generation 1350 (E) and generation 1820 (F). The decrease in heteroplasmy in B1 and B2 gametes 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). From generations 1350–1820, the proportion of heteroplasmic B1 and B2 gametes decreases (C and D) but the level of heteroplasmy increases (compare E with F). This more than offsets the decrease in the proportion of heteroplasmic cells and continues to decrease (A). Around generation 1350, B2 gametes homoplasmic for mutant mitochondria begin to appear, which causes to increase and eventually converge with .

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 gamete types.Parameters: n = 20, μ = 10−4, ch = 0.2 and concave fitness. U1 gametes appear at generation 0, which is the point at which the B1 and B2 gametes reach mutation-selection equilibrium. (A) Relative advantage of each gamete through time (see Model for details). For B-F, the relative proportion is the sum of a particular gamete type (e.g. a homoplasmic wild type U1 gamete) divided by the sum of all cells carrying that allele (all gametes carrying the U1 allele). Thus, the relative proportion describes how an allele is distributed across different gamete types but it does not show their actual frequencies in the population. The heteroplasmic category combines all gametes with any level of heteroplasmy. B-D show the distribution of gametes carrying the U1 allele (B), B1 allele (C) and the B2 allele (D). E-F show a more detailed distribution of gametes carrying the B1 allele at generation 1350 (E) and generation 1820 (F). The decrease in heteroplasmy in B1 and B2 gametes 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). From generations 1350–1820, the proportion of heteroplasmic B1 and B2 gametes decreases (C and D) but the level of heteroplasmy increases (compare E with F). This more than offsets the decrease in the proportion of heteroplasmic cells and  continues to decrease (A). Around generation 1350, B2 gametes homoplasmic for mutant mitochondria begin to appear, which causes  to increase and eventually converge with .
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4400020&req=5

pgen.1005112.g003: Fitness and distribution of gamete types.Parameters: n = 20, μ = 10−4, ch = 0.2 and concave fitness. U1 gametes appear at generation 0, which is the point at which the B1 and B2 gametes reach mutation-selection equilibrium. (A) Relative advantage of each gamete through time (see Model for details). For B-F, the relative proportion is the sum of a particular gamete type (e.g. a homoplasmic wild type U1 gamete) divided by the sum of all cells carrying that allele (all gametes carrying the U1 allele). Thus, the relative proportion describes how an allele is distributed across different gamete types but it does not show their actual frequencies in the population. The heteroplasmic category combines all gametes with any level of heteroplasmy. B-D show the distribution of gametes carrying the U1 allele (B), B1 allele (C) and the B2 allele (D). E-F show a more detailed distribution of gametes carrying the B1 allele at generation 1350 (E) and generation 1820 (F). The decrease in heteroplasmy in B1 and B2 gametes 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). From generations 1350–1820, the proportion of heteroplasmic B1 and B2 gametes decreases (C and D) but the level of heteroplasmy increases (compare E with F). This more than offsets the decrease in the proportion of heteroplasmic cells and continues to decrease (A). Around generation 1350, B2 gametes homoplasmic for mutant mitochondria begin to appear, which causes to increase and eventually converge with .
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.