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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.


Uniparental inheritance replaces biparental inheritance for all tested parameter values.(A) The three fitness functions when ch = 1. Unless indicated otherwise, the parameters for B-F are n = 20, μ = 10−7, ch = 0.2 and concave fitness. (B)U1 replaces B1. (C)U1 takes longer to replace B1 as n increases. (D)U1 takes longer to replace B1 as μ decreases. (E)U1 replaces B1 under all three fitness functions. (F) Number of generations for U1 to replace B1 across a range of costs of heteroplasmy. U1 replaces B1 even if the cost of heteroplasmy is extremely low.
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pgen.1005112.g001: Uniparental inheritance replaces biparental inheritance for all tested parameter values.(A) The three fitness functions when ch = 1. Unless indicated otherwise, the parameters for B-F are n = 20, μ = 10−7, ch = 0.2 and concave fitness. (B)U1 replaces B1. (C)U1 takes longer to replace B1 as n increases. (D)U1 takes longer to replace B1 as μ decreases. (E)U1 replaces B1 under all three fitness functions. (F) Number of generations for U1 to replace B1 across a range of costs of heteroplasmy. U1 replaces B1 even if the cost of heteroplasmy is extremely low.

Mentions: To explore whether a cost to heteroplasmy could have led to the evolution of uniparental inheritance, we study several scenarios. We first examine the simplest case, where mutations in mitochondria are neither advantageous nor disadvantageous (neutral mutations), but heteroplasmic cells incur a fitness cost proportional to the degree of heteroplasmy. Because no empirical data relate fitness to the degree of heteroplasmy, we consider three forms of fitness function to describe selection against heteroplasmy: concave, linear and convex (Fig 1A). For each fitness function, we vary the cost of heteroplasmy (ch), given by ch = 1 − h where h is the fitness of the most heteroplasmic cell in the population, to see how this affects the spread of U1. We generate the concave fitness function byw(i)={1−ch(in/2)2for0≤i<n/2,1−ch(n−in/2)2forn/2≤i≤n,the linear function byw(i)={1−ch(in/2)for0≤i<n/2,1−ch(n−in/2)forn/2≤i≤n,and the convex function byw(i)={1−chin/2for0≤i<n/2,1−chn−in/2forn/2≤i≤n.


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

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

Uniparental inheritance replaces biparental inheritance for all tested parameter values.(A) The three fitness functions when ch = 1. Unless indicated otherwise, the parameters for B-F are n = 20, μ = 10−7, ch = 0.2 and concave fitness. (B)U1 replaces B1. (C)U1 takes longer to replace B1 as n increases. (D)U1 takes longer to replace B1 as μ decreases. (E)U1 replaces B1 under all three fitness functions. (F) Number of generations for U1 to replace B1 across a range of costs of heteroplasmy. U1 replaces B1 even if the cost of heteroplasmy is extremely low.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4400020&req=5

pgen.1005112.g001: Uniparental inheritance replaces biparental inheritance for all tested parameter values.(A) The three fitness functions when ch = 1. Unless indicated otherwise, the parameters for B-F are n = 20, μ = 10−7, ch = 0.2 and concave fitness. (B)U1 replaces B1. (C)U1 takes longer to replace B1 as n increases. (D)U1 takes longer to replace B1 as μ decreases. (E)U1 replaces B1 under all three fitness functions. (F) Number of generations for U1 to replace B1 across a range of costs of heteroplasmy. U1 replaces B1 even if the cost of heteroplasmy is extremely low.
Mentions: To explore whether a cost to heteroplasmy could have led to the evolution of uniparental inheritance, we study several scenarios. We first examine the simplest case, where mutations in mitochondria are neither advantageous nor disadvantageous (neutral mutations), but heteroplasmic cells incur a fitness cost proportional to the degree of heteroplasmy. Because no empirical data relate fitness to the degree of heteroplasmy, we consider three forms of fitness function to describe selection against heteroplasmy: concave, linear and convex (Fig 1A). For each fitness function, we vary the cost of heteroplasmy (ch), given by ch = 1 − h where h is the fitness of the most heteroplasmic cell in the population, to see how this affects the spread of U1. We generate the concave fitness function byw(i)={1−ch(in/2)2for0≤i<n/2,1−ch(n−in/2)2forn/2≤i≤n,the linear function byw(i)={1−ch(in/2)for0≤i<n/2,1−ch(n−in/2)forn/2≤i≤n,and the convex function byw(i)={1−chin/2for0≤i<n/2,1−chn−in/2forn/2≤i≤n.

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.