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.

Fig 1. Geometric definition of terms and concepts.

For a given inheritance class Q (e.g., additivity, dominance, epistasis, etc.; see below), the BLUPs for each strain’s male- (q_M) and female-specific (q_F) variance components from models that were fit separately to male and female data sets represent axes of variation that can be plotted in a bivariate relationship (solid lines). These coordinate systems can be rotated 45° (see Materials and methods) to derive the SA (q_SA) and SC (q_SC) dimensions (dashed lines) for each inheritance class. BLUP, best linear unbiased prediction; SA, sexually antagonistic; SC, sexually concordant.

Fig 2. Graphical representation of variance partitioning.

Variance components (σ², ± 1 s.e.) for fitness estimated by REML. The data underlying all figures and tables can be found in S1 Data. asymm., asymmetric; eff., effects; epi., epistasis; REML, restricted maximum likelihood; s.e., standard error.

Fig 3. SSDR of the allelic variation underlying fitness.

(A) The relative amount of recessive allelic variation for fitness in males (${\sigma }_{{P_M,r}_M}$) and females (${\sigma }_{{P_F,r}_F}$) was significantly negatively correlated (${\mathrm{r}}_{{\sigma }_{{P_M,r}_M},{\sigma }_{{P_F,r}_F}}$ = −0.779 [95% CI −0.92 to −0.46], P = 0.0004) across strains (N = 16; units reflect nonstandardized residual fitness from a model that accounted for environmental and epistatic variance), and (B) the same relationship illustrated and analyzed as ranks (i.e., strains ranked in order of their relative “dominance” over one another; ${\mathrm{r}}_{{\sigma }_{{P_M,r}_M},{\sigma }_{{P_F,r}_F}}$: −0.738, P = 0.0016). Strains tended to be enriched with allelic variation for fitness that was dominant in their heterozygous sons but recessive in their heterozygous daughters and vice versa. SSDR, sex-specific dominance reversal.