Sex and Deleterious Mutations

Gordo, Isabel; Campos, Paulo R. A.

doi:10.1534/genetics.108.086637

Cited by 41 publications

(59 citation statements)

References 28 publications

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“…We found that the benefit of sex increased with population size, in agreement with earlier studies (Iles et al 2003;Keightley and Otto 2006;Gordo and Campos 2008;Hartfield et al 2010). Those studies identified Hill-Robertson interference as the principal cause of this pattern.…”

Section: Discussionsupporting

confidence: 92%

“…For example, Muller's ratchet is strongest in small populations that often experience deleterious mutations, whereas the Fisher-Muller effect is strongest in large populations that often experience beneficial mutations. The increase in the strength of the Fisher-Muller effect between beneficial mutations with population size is intuitive because population size (N) affects the beneficial mutation supply rate (NU b ; where U b is the beneficial mutation rate).More surprising is the recent finding from evolutionary simulations that interference between deleterious mutations can, on its own, also generate a large benefit of sex that increases with population size (Otto and Barton 2001;Iles et al 2003;Barton and Otto 2005;Keightley and Otto 2006;Gordo and Campos 2008;Hartfield et al 2010). This finding is surprising because neither Muller's ratchet (Muller 1964;Haigh 1978;Gordo and Charlesworth 2000) nor background selection Kaplan 1994, 1995) is expected to increase in strength with population size.…”

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confidence: 99%

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An Evolving Genetic Architecture Interacts with Hill–Robertson Interference to Determine the Benefit of Sex

et al. 2016

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Sex is ubiquitous in the natural world, but the nature of its benefits remains controversial. Previous studies have suggested that a major advantage of sex is its ability to eliminate interference between selection on linked mutations, a phenomenon known as HillRobertson interference. However, those studies may have missed both important advantages and important disadvantages of sexual reproduction because they did not allow the distributions of mutational effects and interactions (i.e., the genetic architecture) to evolve. Here we investigate how Hill-Robertson interference interacts with an evolving genetic architecture to affect the evolutionary origin and maintenance of sex by simulating evolution in populations of artificial gene networks. We observed a long-term advantage of sexequilibrium mean fitness of sexual populations exceeded that of asexual populations-that did not depend on population size. We also observed a short-term advantage of sex-sexual modifier mutations readily invaded asexual populations-that increased with population size, as was observed in previous studies. We show that the long-and short-term advantages of sex were both determined by differences between sexual and asexual populations in the evolutionary dynamics of two properties of the genetic architecture: the deleterious mutation rate (U d ) and recombination load (L R ). These differences resulted from a combination of selection to minimize L R ; which is experienced only by sexuals, and Hill-Robertson interference experienced primarily by asexuals. In contrast to the previous studies, in which Hill-Robertson interference had only a direct impact on the fitness advantages of sex, the impact of Hill-Robertson interference in our simulations was mediated additionally by an indirect impact on the efficiency with which selection acted to reduce U d : KEYWORDS evolution of sex; gene network; deleterious mutation rate; recombination load; population size T HE vast majority of organisms alive today have experienced some form of genetic exchange, or sex, in their recent evolutionary history, despite substantial costs (Weismann 1887;Maynard Smith 1978;Bell 1982;Otto and Lenormand 2002). Sex breaks up favorable genetic combinations and increases the risk of transmission of pathogens and selfish genetic elements. Sexual reproduction is often slower than asexual reproduction. In many sexually reproducing eukaryotes, sex involves costs of finding and attracting a mate and of mating in itself; in anisogamous species, if one sex contributes little to progeny production, sexual reproduction carries a twofold cost of producing that sex. The ubiquity of sex implies that it must confer considerable benefits to overcome these costs. However, the nature of these benefits is not well understood. In fact, .20 hypotheses have been proposed to explain the benefits of sex (Bell 1982;Kondrashov 1993;Hurst and Peck 1996;Otto and Lenormand 2002). While hypotheses predicting direct benefits exist [e.g., improved DNA repair (Bernstein et al. 1985)], t...

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Section: Discussionsupporting

confidence: 92%

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confidence: 99%

An Evolving Genetic Architecture Interacts with Hill–Robertson Interference to Determine the Benefit of Sex

et al. 2016

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“…Strong modifiers that substantially increased the sex rate exhibited a higher advantage than weak modifiers. This result was the same as in haploids, in which the advantage of a sex (recombination) modifier begins to increase as its strength increases at p sex E0.01 (Gordo and Campos, 2008).…”

Section: Selection On a Recombination Modifiersupporting

confidence: 59%

“…However, Otto (2003) did not investigate the effects of finite population size on the evolution of sex, which is a potentially important factor that affects selection for segregation. In finite populations, the interaction between drift and selection strongly favors a recombination modifier (Keightley and Otto, 2006;Gordo and Campos, 2008). Nevertheless, the mechanism by which drift influences the conditions favoring segregation remains elusive.…”

Section: Introductionmentioning

confidence: 99%

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

Jiang

et al. 2013

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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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“…Second, our analysis has focused on asexual populations and neglected recombination. Since even weak recombination has the potential to significantly slow Muller's ratchet, it would be interesting to generalize our dynamic balance to include its effects (Bell 1998;Gordo and Campos 2008). Increasing recombination rates would presumably allow the population to maintain better-adapted genotypes in this steady state.…”

Section: Discussionmentioning

confidence: 99%

Dynamic Mutation–Selection Balance as an Evolutionary Attractor

et al. 2012

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The vast majority of mutations are deleterious and are eliminated by purifying selection. Yet in finite asexual populations, purifying selection cannot completely prevent the accumulation of deleterious mutations due to Muller's ratchet: once lost by stochastic drift, the most-fit class of genotypes is lost forever. If deleterious mutations are weakly selected, Muller's ratchet can lead to a rapid degradation of population fitness. Evidently, the long-term stability of an asexual population requires an influx of beneficial mutations that continuously compensate for the accumulation of the weakly deleterious ones. Hence any stable evolutionary state of a population in a static environment must involve a dynamic mutation-selection balance, where accumulation of deleterious mutations is on average offset by the influx of beneficial mutations. We argue that such a state can exist for any population size N and mutation rate U and calculate the fraction of beneficial mutations, e, that maintains the balanced state. We find that a surprisingly low e suffices to achieve stability, even in small populations in the face of high mutation rates and weak selection, maintaining a well-adapted population in spite of Muller's ratchet. This may explain the maintenance of mitochondria and other asexual genomes. P URIFYING selection maintains well-adapted genotypes in the face of deleterious mutations ). Yet in asexual populations, random genetic drift in the most-fit class of individuals will occasionally lead to its irreversible extinction, a process known as Muller's ratchet (Muller 1964;Felsenstein 1974). The repetitive action of the ratchet leads to the accumulation of deleterious mutations, despite the action of purifying selection. This ratchet effect has been extensively analyzed (Gessler 1995;Charlesworth and Charlesworth 1997; Gordo and Charlesworth 2000a,b; and has been observed in experiments (Chao 1990;Duarte et al. 1992;Andersson and Hughes 1996;Zeyl et al. 2001) and in nature (Rice 1994;Lynch 1996;Howe and Denver 2008). In small populations when deleterious mutation rates are high or selection pressures are weak, the ratchet can proceed quickly, causing rapid degradation of asexual genomes Lynch et al. , 1995. Hence Muller's ratchet has been described as a central problem for the maintenance of asexual populations such as mitochondria (Loewe 2006). Avoiding this mutational catastrophe is thought to be a major benefit of sex and recombination (see Barton and Charlesworth 1998 and De Visser and Elena 2007 for reviews).However, new studies indicate that natural and laboratory asexual populations do not always melt down as predicted. For example, recently showed that even very small laboratory populations of phage with high mutation rates tend toward fitness plateaus. In addition, a recent comparison of human, chimpanzee, and rhesus Y chromosomes demonstrated that after an initial period of degradation following the halt of recombination, gene loss in the human Y chromosome effectively stopped (Hughes et al. 2...

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Sex and Deleterious Mutations

Cited by 41 publications

References 28 publications

An Evolving Genetic Architecture Interacts with Hill–Robertson Interference to Determine the Benefit of Sex

An Evolving Genetic Architecture Interacts with Hill–Robertson Interference to Determine the Benefit of Sex

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

Dynamic Mutation–Selection Balance as an Evolutionary Attractor

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