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Sex-specific dominance reversal of genetic variation for fitness.

ABSTRACT: The maintenance of genetic variance in fitness represents one of the most longstanding enigmas in evolutionary biology. Sexually antagonistic (SA) selection may contribute substantially to maintaining genetic variance in fitness by maintaining alternative alleles with opposite fitness effects in the two sexes. This is especially likely if such SA loci exhibit sex-specific dominance reversal (SSDR)-wherein the allele that benefits a given sex is also dominant in that sex-which would generate balancing selection and maintain stable SA polymorphisms for fitness. However, direct empirical tests of SSDR for fitness are currently lacking. Here, we performed a full diallel cross among isogenic strains derived from a natural population of the seed beetle Callosobruchus maculatus that is known to exhibit SA genetic variance in fitness. We measured sex-specific competitive lifetime reproductive success (i.e., fitness) in >500 sex-by-genotype F1 combinations and found that segregating genetic variation in fitness exhibited pronounced contributions from dominance variance and sex-specific dominance variance. A closer inspection of the nature of dominance variance revealed that the fixed allelic variation captured within each strain tended to be dominant in one sex but recessive in the other, revealing genome-wide SSDR for SA polymorphisms underlying fitness. Our findings suggest that SA balancing selection could play an underappreciated role in maintaining fitness variance in natural populations.

SUBMITTER: Grieshop K

PROVIDER: S-EPMC6303075 | biostudies-literature | 2018 Dec

REPOSITORIES: biostudies-literature

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Sex-specific dominance reversal of genetic variation for fitness.

Grieshop Karl K Arnqvist Göran G

PLoS biology 20181211 12

The maintenance of genetic variance in fitness represents one of the most longstanding enigmas in evolutionary biology. Sexually antagonistic (SA) selection may contribute substantially to maintaining genetic variance in fitness by maintaining alternative alleles with opposite fitness effects in the two sexes. This is especially likely if such SA loci exhibit sex-specific dominance reversal (SSDR)-wherein the allele that benefits a given sex is also dominant in that sex-which would generate bala ...[more]

PMID: 30533008

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Project description:Sex differences in morphology, physiology, development, and behavior are widespread, yet the sexes inherit nearly identical genomes, causing most traits to exhibit strong and positive cross-sex genetic correlations. In contrast to most other traits, estimates of cross-sex genetic correlations for fitness and fitness components ( r W fm ) are generally low and occasionally negative, implying that a substantial fraction of standing genetic variation for fitness might be sexually antagonistic (i.e., alleles benefitting one sex harm the other). Nevertheless, while low values of r W fm are often regarded as consequences of sexually antagonistic selection, it remains unclear exactly how selection and variation in quantitative traits interact to determine the sign and magnitude of r W fm , making it difficult to relate empirical estimates of cross-sex genetic correlations to the evolutionary processes that might shape them. We present simple univariate and multivariate quantitative genetic models that explicitly link patterns of sex-specific selection and trait genetic variation to the cross-sex genetic correlation for fitness. We show that r W fm provides an unreliable signal of sexually antagonistic selection for two reasons. First, r W fm is constrained to be less than the cross-sex genetic correlation for traits affecting fitness, regardless of the nature of selection on the traits. Second, sexually antagonistic selection is an insufficient condition for generating negative cross-sex genetic correlations for fitness. Instead, negative fitness correlations between the sexes ( r W fm < 0 ) can only emerge when selection is sexually antagonistic and the strength of directional selection on each sex is strong relative to the amount of shared additive genetic variation in female and male traits. These results imply that empirical tests of sexual antagonism that are based on estimates of r W fm will be conservative and underestimate its true scope. In light of these theoretical results, we revisit current data on r W fm and sex-specific selection and find that they are consistent with the theory.

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Sex-specific dominance reversal of genetic variation for fitness.

Publications

Sex-specific dominance reversal of genetic variation for fitness.

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