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Evolution of sex

Resolving the paradox of sex and recombination

Nature Reviews Genetics volume 3, pages 252–261 (2002)Cite this article

Key Points

  • One of the most enduring puzzles in evolutionary biology is why sexual reproduction, whereby the genomes of different individuals are mixed together, is so widespread.

  • Theoretical analyses have shown that genome mixing is a risky endeavour, and the conditions that favour the evolution of high rates of sex and recombination are often quite restrictive.

  • Most previous mathematical models have, however, focused on populations that are infinite in size, unstructured and isolated from other species.

  • By incorporating realistic complexities, including species interactions, spatial structure and genetic drift, recent studies have broadened the conditions under which high rates of sex and recombination are expected to evolve.

Abstract

Sexual reproduction and recombination are ubiquitous. However, a large body of theoretical work has shown that these processes should only evolve under a restricted set of conditions. New studies indicate that this discrepancy might result from the fact that previous models have ignored important complexities that face natural populations, such as genetic drift and the spatial structure of populations.

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Figure 1: The percentage change in recombination after a period of strong selection.
Figure 2: Conditions under which an allele that modifies the probability of sexual reproduction will spread by increasing the segregation of alleles at a selected locus.
Figure 3: The proportional change in the frequency of sex as a function of population size after 50 generations of selection in a three-locus haploid model.

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Acknowledgements

The authors gratefully acknowledge the comments and suggestions of J. Boughman, C. Griswold, T. Johnson, R. Redfield, H. Rundle, R. Sargent, D. Schluter, M. Whitlock and three anonymous reviewers. Funding was provided by the Natural Sciences and Engineering Research Council (Canada) to S.P.O. and the Centre National de la Recherche Scientifique (France) to S.P.O. and T. L.

Author information

Authors and Affiliations

  1. Department of Zoology, University of British Columbia, 6270 University Boulevard, Vancouver, V6T 124, British Columbia, Canada

    Sarah P. Otto

  2. Centre d'Ecologie Functionnelle et Evolutive, Centre National de la Recherche Scientifique, 1919 Route de Mende, Montpellier, 34293 Cedex 5, France

    Thomas Lenormand

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  1. Sarah P. Otto
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Corresponding author

Correspondence to Sarah P. Otto.

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FURTHER INFORMATION

Deinococcus radiodurans

Rickettsia prowazekii

Sarah Otto's lab

Glossary

TRANSDUCTION

The exchange of genetic material from one cell to another that is mediated by a virus or phage.

TRANSFORMATION

The uptake of DNA by a bacterium from the surrounding environment.

CONJUGATION

In prokaryotes, the transfer of DNA from a donor cell to a recipient cell that is mediated by direct cell–cell contact.

PROTIST

A eukaryote other than animals, plants and fungi; often single celled.

CHIASMA

(pl. chiasmata). The cytological manifestation of genetic exchange between chromosomes, indicating that a crossover has occurred between homologous chromosomes.

ANEUPLOIDY

The presence of extra copies, or fewer copies, of some chromosomes.

EQUILIBRIUM

A state in which a system remains unchanged over time.

LINKAGE DISEQUILIBRIUM

(D). A measure of genetic associations between alleles at different loci, which indicates whether particular haplotypes are more common than expected. We use the two-locus measure, D = frequency(AB) × frequency(ab) − frequency(Ab) × frequency(aB).

HAPLOTYPE

A haploid genotype. A diploid genotype comprises a maternal and a paternal haplotype.

GENETIC DRIFT

(also known as random drift). A phenomenon whereby the frequency of a gene in a population changes over time because the number of offspring born to parents that carry the gene is subject to chance variation.

EPISTASIS

(ɛ). A measure of fitness interactions between alleles at different loci. In haploids, we use the two-locus measure, ɛ = fitness(AB) × fitness(ab) − fitness(Ab) × fitness(aB).

MUTATION–SELECTION BALANCE

The equilibrium at which selection that increases the frequency of a favourable allele exactly balances mutations that decrease the frequency.

SELECTION COEFFICIENT

A term that describes the difference in average fitness between two genotypes when fitness is measured relative to the average fitness of one of the genotypes (known as the reference genotype).

DIRECTIONAL SELECTION

Selection that favours one allele over all other alleles of a gene. The frequency of this beneficial allele can rise or can be held in check by recurrent mutation.

RECOMBINATION LOAD

The difference in fitness between offspring produced without recombination and those produced with recombination.

HARDY–WEINBERG EQUILIBRIUM

A state in which the frequency of each diploid genotype at a locus equals that expected from the random union of alleles — that is, where the inbreeding coefficient (F) is zero.

INBREEDING COEFFICIENT

(F). A measure of genetic associations between alleles at the same locus, which indicates whether homozygotes (positive F) or heterozygotes (negative F) are more common than expected. For ease of comparison with linkage disequilibrium, we write the standard measure for F as {frequency(AA) × frequency(aa) − [0.5 × frequency(Aa)]2}/{frequency(A) × frequency(a)}.

DOMINANCE COEFFICIENT

The factor by which the selection coefficient is reduced in heterozygotes relative to homozygotes.

SINGLE-LOCUS INTERACTION

(ı). A measure of fitness interactions between alleles at the same locus. We use the single-locus measure, ı = fitness(AA) × fitness(aa) − fitness(Aa)2.

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Otto, S., Lenormand, T. Resolving the paradox of sex and recombination. Nat Rev Genet 3, 252–261 (2002). https://doi.org/10.1038/nrg761

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