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The evolution of sex: empirical insights into the roles of epistasis and drift

Nature Reviews Genetics volume 8, pages 139–149 (2007)Cite this article

Key Points

  • The origin and maintenance of sexual reproduction is one of the oldest and most intriguing problems in evolutionary biology.

  • Most models assume that the advantage of sex relies on the increased production of genetic variation, which can be used by natural selection. For this to occur, there must be forces that systematically diminish this variation (that is, that cause 'negative linkage disequilibrium'), such as genetic drift or negative epistasis.

  • Recent laboratory-based experiments that use microbes or comparative genomic analyses of microcrustaceans and nematodes have shown the ability of sex to facilitate adaptation and slow down maladaptation, but have not revealed whether drift or epistasis is the main responsible force.

  • Direct and indirect empirical studies of epistasis have been numerous, but have not provided decisive support for negative epistasis.

  • Frustration with the equivocal evidence for negative epistasis has stimulated two recent developments: studies of genetic drift as a cause of low genetic variation, and studies that combine the effects of more than one mechanism (the so-called 'pluralist approaches').

  • Recent in silico studies point at a possible two-way evolutionary relationship between recombination and negative epistasis. By selecting for more robust and modular genomes, sex might promote negative epistasis as well as long-term evolvability. So, sex modulates genome architecture, by which it might forge its own evolution.

Abstract

Despite many years of theoretical and experimental work, the explanation for why sex is so common as a reproductive strategy continues to resist understanding. Recent empirical work has addressed key questions in this field, especially regarding rates of mutation accumulation in sexual and asexual organisms, and the roles of negative epistasis and drift as sources of adaptive constraint in asexually reproducing organisms. At the same time, new ideas about the evolution of sexual recombination are being tested, including intriguing suggestions of an important interplay between sex and genetic architecture, which indicate that sex and recombination could have affected their own evolution.

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Figure 1: Epistasis, linkage disequilibrium and the direct and indirect effects of sex.
Figure 2: The relationship between robustness, redundancy and epistasis.
Figure 3: The relationship between epistasis and genome complexity.

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Acknowledgements

J.A.G.M.d.V. is supported by an Innovational Research Incentives grant from the Netherlands Organization of Scientific Research. S.F.E. is supported by grants from the Spanish Ministerio de Educación y Ciencia-FEDER, the Generalitat Valenciana and the EMBO Young Investigator Program. We thank D. Aanen, F. Debets, R. Hoekstra, A. Kondrashov, S. Otto, J. Peck, R. Sanjuán and C. Zeyl for comments and discussion.

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Authors and Affiliations

  1. Laboratory of Genetics, Wageningen University, Wageningen, 6703 BD, The Netherlands

    J. Arjan G. M. de Visser

  2. Instituto de Biología Molecular y Celular de Plantas, Consejo Superior de Investigaciones Científicas-UPV, València, 46022, Spain

    Santiago F. Elena

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Glossary

Recombinational load

A decrease in mean fitness due to the break up of co-adapted (that is, epistatic) gene combinations by recombination.

Drift

A change in genotype frequencies due to chance variation. Also known as random or genetic drift.

Epistasis

Deviation from independent (that is, multiplicative) gene action on a polygenically encoded phenotype, or on fitness.

Anisogamy

The condition in which the male and female gametes are of different sizes.

Sexual selection

Selection among individuals of one sex that is exerted through competition for mates, or through the mating preference of the opposite sex.

Directional selection

Natural selection that promotes the continued change of a phenotype in one direction.

Linkage disequilibrium

Deviation in a population from a random distribution of alleles at different loci, denoted by D. D < 0 reflects the relative absence of individuals with particular allele combinations, D > 0 reflects the relative abundance of such individuals.

Stabilizing selection

A form of selection that results in intermediate phenotypes having greater fitness than extreme phenotypes.

Fisher–Muller hypothesis

The theory that, through recombination, sex speeds up adaptation by bringing together beneficial mutations that have arisen in different genetic backgrounds.

Muller's ratchet

The process by which the genome of an asexual population accumulates deleterious mutations in an irreversible manner, owing to the chance loss of individuals with the lowest number of mutations.

Background selection

The interfering effect of selection against deleterious mutations at loci that are linked to another locus that is under positive selection.

Segmented bacteriophage

A bacterial virus that has a genome that is divided into several fragments (chromosomes), which can be encapsidated into either the same or different viral particles, and allows reassortment of segments in co-infected bacteria.

Selective interference

The situation in which the fixation of an allele at a locus affects the probability of fixation of alleles at other linked loci.

Digital organisms

Computer-generated organisms that mutate and evolve inside the memory of a computer, where they compete for CPU time, on which they depend for their replication.

Mutational meltdown

The process by which small populations accumulate deleterious mutations leading to loss of fitness and a concomitant decline in effective population size. The decline in population size further accelerates Muller's ratchet and enhances the likelihood of extinction.

Purifying selection

Selection against deleterious alleles.

Clonal interference

Competition between multiple beneficial mutations that have arisen in different individuals in an asexual population.

Isogenic

Genetically identical.

Fitness components

All the traits of an organism that contribute to its reproductive success.

Compensatory mutation

A mutation that has a beneficial effect that depends on the presence of a deleterious mutation at another locus.

Truncation selection

A form of selection such that individuals with a phenotype below or above a certain threshold have a relative fitness of zero or one, respectively.

Deme

A local population of organisms of a sexual species that actively interbreed with one another and share a distinct gene pool.

Robustness

The invariance of a phenotype or fitness in the face of genetic perturbations (for example, mutations) or environmental perturbations.

Evolvability

The long-term ability of a population or lineage to evolve new adaptive changes and prevent extinction.

Modularity

A specific form of genome architecture in which organismal or sub-organismal functions are encoded by discrete, contiguous parts of the genome.

Pleiotropic constraint

Evolutionary constraint that is caused when a gene that is under selection due to a positive effect on one trait has simultaneous negative side effects on other traits, which limit or prevent its selection.

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de Visser, J., Elena, S. The evolution of sex: empirical insights into the roles of epistasis and drift. Nat Rev Genet 8, 139–149 (2007). https://doi.org/10.1038/nrg1985

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