Recent advances in understanding of the evolution and maintenance of sex

Hurst, Laurence D.; Peck, Joel R.

doi:10.1016/0169-5347(96)81041-x

Cited by 330 publications

(289 citation statements)

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“…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)], the main benefits of sex are believed to be indirect, such as increased evolvability (Weismann 1887;Maynard Smith 1978;Bell 1982;Kondrashov 1993;Burt 2000;Otto and Lenormand 2002).…”

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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

et al. 2016

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“…However, sex also can facilitate adaptive evolution regardless of random drift, as long as fitness grows at less than an exponential rate with the number of beneficial alleles in the genotype, which must be the case as fitness cannot approach infinity (5,6). Thus, sex is thought to speed up allele replacements driven by directional selection under a broad range of plausible conditions, although the importance of this effect for the evolution of sex remains controversial (7)(8)(9)(10)(11)(12).…”

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“…(b) A continuous fitness ridge used in our simulations. (c) A discontinuous fitness ridge such that, to evolve from the phenotype (10,10) to the phenotype (11,11), a population must acquire two alleles 1 that are individually deleterious.…”

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Multidimensional epistasis and the disadvantage of sex

Kondrashov

2001

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

117

111

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Sex is thought to facilitate accumulation of initially rare beneficial mutations by allowing simultaneous allele replacements at many loci. However, this advantage of sex depends on a restrictive assumption that the fitness of a genotype is determined by fitness potential, a single intermediate variable to which all loci contribute additively, so that new alleles can accumulate in any order. Individual-based simulations of sexual and asexual populations reveal that under generic selection, sex often retards adaptive evolution. When new alleles are beneficial only if they accumulate in a prescribed order, a sexual population may evolve two or more times slower than an asexual population because only asexual reproduction allows some overlap of successive allele replacements. Many other fitness surfaces lead to an even greater disadvantage of sex. Thus, either sex exists in spite of its impact on the rate of adaptive allele replacements, or natural fitness surfaces have rather specific properties, at least at the scale of intrapopulation genetic variability.

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“…However, 'little sex' seems to be sufficient for avoiding the accumulation of mutations and for maintaining genetic variability (Hurst and Peck, 1996). As such, strictly asexual taxa are very rare and most do not completely avoid sexual reproduction, which could be the key to their long persistence.…”

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confidence: 99%