The Role of Advantageous Mutations in Enhancing the Evolution of a Recombination Modifier

Hartfield, Matthew; Otto, Sarah P.; Keightley, Peter D.

doi:10.1534/genetics.109.112920

Cited by 43 publications

(77 citation statements)

References 78 publications

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“…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%

“…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%

“…O. B. Whitlock et al Hartfield et al 2010). The deleterious mutation rate, the distribution of mutational effects, and the epistatic interactions between mutations are all properties of the genetic architecture (Box 1) that are known to play an important role in the indirect benefits of sex (Kondrashov 1982(Kondrashov , 1988Charlesworth 1990;Otto and Feldman 1997).…”

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

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“…Relative effects of segregation and recombination X Jiang et al contrast, smaller N e impedes the spread rate of the sex modifier (Hartfield et al, 2010). The decrease in u/u* was attributed to the dominance of the opposite effects of delaying the spread rate of the modifier exceeding the effects of increasing interference.…”

Section: Selection On a Recombination Modifiermentioning

confidence: 98%

“…The simulation programs used in this study (written in C þ þ and available upon request) were somewhat similar to those in haploid models used by Hartfield et al (2010), but our simulations were newly established. In both studies, an infinite number of possible alleles at each locus, the absence of epistasis and no dominance in mutations were considered.…”

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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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Ecological differentiation facilitates fine‐scale coexistence of sexual and asexual Boechera

Rushworth

Windham

Keith

et al. 2018

American J of Botany

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Premise of the study: Ecological differentiation (ED) between sexual and asexual organisms may permit the maintenance of reproductive polymorphism. Several studies of sexual/asexual ED in plants have shown that the geographic ranges of asexuals extend beyond those of sexuals, often in areas of higher latitude or elevation. But very little is known about ED at fine scales, wherein coexistence of sexuals and asexuals may be permitted by differential niche occupation. Methods: We used 149 populations of sexual and apomictic lineages in the genus Boechera (rock cress) collected across a portion of this mustard’s vast range. We characterized reproductive mode, ploidy, and species identity or hybrid parentage of each individual, and then used a multi-pronged statistical approach to 1) identify ED between sexuals and asexuals; 2) investigate the impacts of two confounding factors, polyploidy and hybridization, on ED; and 3) determine the environmental variables underlying ED. Key results: We found that sexuals and asexuals are significantly ecologically differentiated across the landscape, despite fine-scale interdigitation of these two reproductive forms. Asexual reproduction was strongly associated with greater disturbance, reduced slope, and greater environmental variability. Although ploidy had little effect on the patterns observed, hybridization has a unique impact on the relationships between asexual reproduction and specific environmental variables. Conclusions: Ecological differentiation along the axes of disturbance, slope, and climatic variability, as well as the effects of heterozygosity, may contribute to the maintenance of sexuality and asexuality across the landscape, ultimately impacting the establishment and spread of asexual lineages.

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The Role of Advantageous Mutations in Enhancing the Evolution of a Recombination Modifier

Cited by 43 publications

References 78 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

Ecological differentiation facilitates fine‐scale coexistence of sexual and asexual Boechera

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