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Population genetics of sexual conflict in the genomic era

Key Points

  • Case studies on several loci with sexually antagonistic alleles, identified by genetic and genomic approaches, reveal that sexual conflict leads to balancing selection to maintain both female-benefit and male-benefit alleles.

  • The signature of balancing selection from population genetic data is increasingly useful in assessing the amount and distribution of sexual conflict within the genome.

  • The causes of sexual conflict remain unclear, and multiple population genetic tools must be combined to determine whether sexual conflict results primarily from reproductive success or survival.

  • Sexual conflict can be resolved through a variety of mechanisms. However, balancing selection is only relaxed when sexual conflict is fully resolved.

Abstract

Sexual conflict occurs when selection acts in opposing directions on males and females. Case studies in both vertebrates and invertebrates indicate that sexual conflict maintains genetic diversity through balancing selection, which might explain why many populations show more genetic variation than expected. Recent population genomic approaches based on different measures of balancing selection have suggested that sexual conflict can arise over survival, not just reproductive fitness as previously thought. A fuller understanding of sexual conflict will provide insight into its contribution to adaptive evolution and will reveal the constraints it might impose on populations.

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Figure 1: Case studies of balancing selection and sexual conflict.
Figure 2: Population genomics measures of sexual conflict.
Figure 3: Differential effects of sexual conflict and sex-specific selection on FST for a two-allele locus.

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Acknowledgements

The author is grateful for generous support from the European Research Council (grant agreements 260233 and 680951) and a Royal Society Wolfson Merit Award. The author thanks P. Almeida, M. Bentley, I. Darolti, J. Morris, V. Oostra, S. Sumner, B. Taylor and D. Taylor for helpful comments and suggestions on a previous draft of this manuscript, the referees for their helpful suggestions, A. Wright and M. Fumagalli for stimulating discussions, and N. Wedell and S. Johnston for their expertise.

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PowerPoint slides

Glossary

Inter-locus sexual conflict

The result of evolutionary antagonistic interactions between males and females for alleles at two or more loci. In this form of sexual conflict, adaptation at one locus that favours one sex at some cost to the other is followed by counter-adaptations at a different locus for the harmed sex. The cycle of adaptation and counter-adaptation can repeat many times, resulting in an arms race between males and females.

Intra-locus sexual conflict

The result of conflicting selection pressures for males and females over alleles at a single locus. In this form of sexual conflict, alleles at a single locus have opposing effects on male and female fitness.

Genetic architecture

The underlying genetic basis of a phenotypic trait and, in particular, the genetic basis for phenotypic variation in the trait.

Reproductive fitness

The reproductive success, such as the number of viable offspring, of a given genotype. It is typically measured by the average contribution of the genotype to the next generation of the population compared to other genotypes.

Positive selection

Selection to increase the frequency of a new advantageous mutation within a population.

Purifying selection

Removal of deleterious variation from a population by selection.

Balancing selection

The evolutionary process whereby more alleles are maintained in a population than would be expected from the mutation rate and population size. It results from fluctuating selection (that is, changes in the direction of selection) over time, space or, in this case, sex.

Viability

The proportion of embryos with a given genotype that survive development.

Candidate gene

A pre-specified gene of interest based on its known function.

Transcriptome analysis

A technique in which the RNA levels are compared between treatment and control groups for all coding genes in the genome.

Genome-wide association studies

(GWAS). Studies based on a statistical method to determine what regions of the genome are associated with a trait of interest.

Microsatellite

A short nucleotide repeat at a particular region of a chromosome. Microsatellites often have many alleles within a population, each of which has a different number of repeats.

Heterozygote advantage

A phenomenon in which the presence of two different alleles at a given locus confers increased reproductive fitness compared to either homozygote. Also referred to as heterosis or overdominance.

Dominance reversal

A switch in the dominance–recessivity relationship of an allele between different groups, in this case between males and females.

Beavis effect

A phenomenon in quantitative genetic studies in which the effect sizes of significant quantitative trait loci are overestimated and those of nonsignificant quantitative trait loci are underestimated. Because significance is related to sample size, the Beavis effect implies that identifying small but significant effects on fitness will require very large samples that are often not feasible in laboratory or natural populations.

Tajima's D

A measure of the proportion of polymorphic sites within a given locus or of the percentage of segregating sites.

Fixation index

(FST). A measure of differences in allele frequency between two groups, typically owing to genetic structure. In the context of comparing males and females from a single population, FST can result from differences in survival or viability.

Hardy–Weinberg equilibrium

A fundamental principle of population genetics that predicts that allele and genotype frequencies at a given locus will remain constant in a population in the absence of other evolutionary influences.

Mortality load

The proportion of individuals in a cohort that die before reproduction.

Sex-biased genes

Genes that are more highly expressed in one sex than the other.

Selective sweep

The reduction or elimination of genetic variation near a beneficial allele that has recently been fixed in a population due to strong positive selection. Sweeps are the result of genetic linkage between the beneficial mutation and nearby variation.

Hemizygous

The state of having only one copy of a chromosome in an otherwise diploid organism. Hemizygosity occurs most frequently on the sex chromosomes, where the heterogametic sex only has one functional copy of X-linked or Z-linked loci.

Pseudo-autosomal region

(PAR). The portion of the sex chromosome that still recombines in the heterogametic sex and is not inherited in a strictly sex-linked manner.

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Mank, J. Population genetics of sexual conflict in the genomic era. Nat Rev Genet 18, 721–730 (2017). https://doi.org/10.1038/nrg.2017.83

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