Accumulation of mutations in sexual and asexual populations

Pamilo, Pekka; Nei, Masatoshi; Li, Wen-Hsiung

doi:10.1017/s0016672300026938

Cited by 143 publications

(142 citation statements)

References 21 publications

(25 reference statements)

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“…Indeed, theoretical studies have shown that slightly deleterious mutations accumulate at a faster rate in asexual genomes than in sexual genomes (38,39). However, if deleterious mutations accumulate continuously in a gene, the gene will eventually deteriorate and lose its original function (39)(40)(41). Note that here we are considering only the genes that still maintain the original function after 200 million or 1.5 billion years of endosymbiosis.…”

Section: Enhanced Mutation Rate and Relaxation Of Selection As Causesmentioning

confidence: 99%

“…Several authors (6)(7)(8)(9)(10) have suggested that the enhanced evolutionary rate observed in genes of Buchnera and organelles can be explained by Muller's ratchet (37,38), which refers to the event that deleterious mutations accumulate in asexual genomes because they cannot be eliminated through recombination. Indeed, theoretical studies have shown that slightly deleterious mutations accumulate at a faster rate in asexual genomes than in sexual genomes (38,39). However, if deleterious mutations accumulate continuously in a gene, the gene will eventually deteriorate and lose its original function (39)(40)(41).…”

Section: Enhanced Mutation Rate and Relaxation Of Selection As Causesmentioning

confidence: 99%

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Acceleration of genomic evolution caused by enhanced mutation rate in endocellular symbionts

Itoh

Martin

Nei

2002

Proc. Natl. Acad. Sci. U.S.A.

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147

109

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Endosymbionts, which are widely observed in nature, have undergone reductive genome evolution because of their long-term intracellular lifestyle. Here we compared the complete genome sequences of two different endosymbionts, Buchnera and a protist mitochondrion, with their close relatives to study the evolutionary rates of functional genes in endosymbionts. The results indicate that the rate of amino acid substitution is two times higher in symbionts than in their relatives. This rate increase was observed uniformly among different functional classes of genes, although strong purifying selection may have counterbalanced the rate increase in a few cases. Our data suggest that, contrary to current views, neither the Muller's ratchet effect nor the slightly deleterious mutation theory sufficiently accounts for the elevated evolutionary rate. Rather, the elevated evolutionary rate appears to be mainly due to enhanced mutation rate, although the possibility of relaxation of purifying selection cannot be ruled out. E ubacteria that live within eukaryotic cells-endocellular symbionts-obtain metabolic precursors synthesized by their hosts and have lost many genes for biosynthetic pathways relative to their free-living cousins (1, 2). Such genome reduction is manifested in Buchnera sp. APS (3, 4), a maternally transmitted obligate ␥-proteobacterial endosymbiont of aphids. This endosymbiont produces essential amino acids for its insect host, which in turn provides nonessential amino acids and other metabolites for the bacterium (1). More extreme genome reduction is observed in mitochondria (2), ATP-producing eukaryotic organelles that stem from endosymbiotic eubacteria and that have relinquished their genome entirely in their anaerobic forms, hydrogenosomes (5).In addition, the rate of amino acid substitution of functional genes is often higher in endosymbionts than in their sister species or bacteria that are considered to be closest to their ancestral species (6-10). This accelerated rate of evolution in endosymbionts is generally believed to occur by Muller's ratchet effect (see below) or by fixation of slightly deleterious mutations in small endosymbiont populations (6-10). However, the acceleration of evolutionary rate may also be caused by a high mutation rate or relaxation of purifying selection in endosymbionts. To distinguish between these two types of hypotheses, we conducted genomic comparison of the endosymbionts Buchnera sp. APS and Reclinomonas americana mitochondrion (mt) with their closest relatives Escherichia coli and Rickettsia prowazekii, respectively, and estimated the relative rates of amino acid substitution for different groups of proteins. Materials and MethodsIdentification of Orthologs. To compare rates of amino acid substitution in endocellular symbionts and relatives, we identified orthologous genes, that is, the genes that were neither duplicated before the divergence of species under study nor horizontally transferred subsequently. We first compared the genome of Buchnera sp. APS with that o...

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Section: Enhanced Mutation Rate and Relaxation Of Selection As Causesmentioning

confidence: 99%

Section: Enhanced Mutation Rate and Relaxation Of Selection As Causesmentioning

confidence: 99%

Acceleration of genomic evolution caused by enhanced mutation rate in endocellular symbionts

Itoh

Martin

Nei

2002

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

147

109

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“…where X = 1 -(1//T) (Gabriel et al, in press;Haigh 1978;Pamilo et al 1987). In this formulation, the mean number of mutations (n) is assumed to be monitored on the adults in each generation that survive selection.…”

Section: An Analytical Approachmentioning

confidence: 99%

“…This phenomenon, now known as Muller's ratchet (Felsenstein 1974), has been subject to numerous theoretical studies with the objective of evaluating the rate at which mean population fitness decays under asexuality (Bell 1988a,b;Birky and Walsh 1988;Charlesworth 1990;Gabriel et al, in press;Haigh 1978;Kondrashov 1982Kondrashov , 1984Lynch and Gabriel 1990;Maynard Smith 1978;Melzer and Koeslag 1991;Pamilo et al 1987). But with few exceptions (Bell 1988a,b;Gabriel et al, in press;Lynch and Gabriel 1990;Melzer and Koeslag 1991), these studies have been pursued under the assumption that population size is unaffected by the accumulation of mutations.…”

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confidence: 99%

The Mutational Meltdown in Asexual Populations

Lynch¹,

Bürger²,

Butcher³

et al. 1993

Journal of Heredity

572

499

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Loss of fitness due to the accumulation of deleterious mutations appears to be inevitable in small, obligately asexual populations, as these are incapable of reconstituting highly fit genotypes by recombination or back mutation. The cumulative buildup of such mutations is expected to lead to an eventual reduction in population size, and this facilitates the chance accumulation of future mutations. This synergistic interaction between population size reduction and mutation accumulation leads to an extinction process known as the mutational meltdown, and provides a powerful explanation for the rarity of obligate asexuality. We give an overview of the theory of the mutational meltdown, showing how the process depends on the demographic properties of a population, the properties of mutations, and the relationship between fitness and number of mutations incurred.

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“…An increasing p sex evidently increased the fixation probability of the sex modifier ( Figure 6). A low probability of sex has been proven to provide substantial benefits in terms of sex rate (Pamilo et al, 1987;Charlesworth et al, 1993;Green and Noakes, 1995;Barton and Charlesworth, 1998). Strong modifiers that substantially increased the sex rate exhibited a higher advantage than weak modifiers.…”

Section: Selection On a Recombination Modifiermentioning

confidence: 99%

Relative effects of segregation and recombination on the evolution of sex in finite diploid populations

Jiang

et al. 2013

Heredity

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The mechanism of reproducing more viable offspring in response to selection is a major factor influencing the advantages of sex. In diploids, sexual reproduction combines genotype by recombination and segregation. Theoretical studies of sexual reproduction have investigated the advantage of recombination in haploids. However, the potential advantage of segregation in diploids is less studied. This study aimed to quantify the relative contribution of recombination and segregation to the evolution of sex in finite diploids by using multilocus simulations. The mean fitness of a sexually or asexually reproduced population was calculated to describe the long-term effects of sex. The evolutionary fate of a sex or recombination modifier was also monitored to investigate the short-term effects of sex. Two different scenarios of mutations were considered: (1) only deleterious mutations were present and (2) a combination of deleterious and beneficial mutations. Results showed that the combined effects of segregation and recombination strongly contributed to the evolution of sex in diploids. If deleterious mutations were only present, segregation efficiently slowed down the speed of Muller's ratchet. As the recombination level was increased, the accumulation of deleterious mutations was totally inhibited and recombination substantially contributed to the evolution of sex. The presence of beneficial mutations evidently increased the fixation rate of a recombination modifier. We also observed that the twofold cost of sex was easily to overcome in diploids if a sex modifier caused a moderate frequency of sex.

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Accumulation of mutations in sexual and asexual populations

Cited by 143 publications

References 21 publications

Acceleration of genomic evolution caused by enhanced mutation rate in endocellular symbionts

Acceleration of genomic evolution caused by enhanced mutation rate in endocellular symbionts

The Mutational Meltdown in Asexual Populations

Relative effects of segregation and recombination on the evolution of sex in finite diploid populations

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