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.
Highlights
One of the most longstanding challenges for evolutionary biologists has been to explain the maintenance of genetic variance in fitness [1,2,3,4,5,6,7]
Antagonistic (SA) genetic variation—in which alternative alleles have opposite fitness effects in the sexes—can generate balancing selection that maintains genetic variation for fitness if the alleles that benefit a given sex are dominant in that sex
We show that the Sexually antagonistic (SA) genetic variation underlying fitness in a well-known seed beetle population exhibits these beneficial reversals of dominance, suggesting SA selection may commonly maintain heritable genetic variation for fitness throughout the genome
Summary
One of the most longstanding challenges for evolutionary biologists has been to explain the maintenance of genetic variance in fitness [1,2,3,4,5,6,7]. The two general hypotheses for explaining this are mutation-selection balance and balancing selection [2,3,4]. Under the former, many polymorphisms throughout the genome are maintained at low allele frequencies because of a constant influx of deleterious mutations [10,11,12,13,14], yet this process cannot singlehandedly explain the extent and pattern of the genetic variance observed in nature [4,5,6,7] (explained below). Some form of balancing selection—including scenarios in which alternative alleles offer fitness benefits in different contexts (e.g., environments, genotypes, seasons, or sexes)—must contribute to the maintenance of polymorphisms for fitness throughout the genome [4,5,6,7]
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