Dominance reversals and the maintenance of genetic variation for fitness

Abstract

Antagonistic selection between different fitness components (e.g., survival versus fertility) or different types of individuals in a population (e.g., females versus males) can potentially maintain genetic diversity and thereby account for the high levels of fitness variation observed in natural populations. However, the degree to which antagonistic selection can maintain genetic variation critically depends on the dominance relations between antagonistically selected alleles in diploid individuals. Conditions for stable polymorphism of antagonistically selected alleles are narrow, particularly when selection is weak, unless the alleles exhibit "dominance reversals"-in which each allele is partially or completely dominant in selective contexts in which it is favored and recessive in contexts in which it is harmful. Although theory predicts that dominance reversals should emerge under biologically plausible conditions, evidence for dominance reversals is sparse. In this primer, we review theoretical arguments and data supporting a role for dominance reversals in the maintenance of genetic variation. We then highlight an illuminating new study by Grieshop and Arnqvist, which reports a genome-wide signal of dominance reversals between male and female fitness in seed beetles.

Fig 1. Dominance reversals promote balancing selection at an SA gene.

Left panel: strong selection. Right panel: weak selection. The regions between the solid black curves show the conditions for balancing selection under parallel dominance (h_f = 1 − h_m). The regions between the dashed lines show the conditions for balancing selection under a partial dominance reversal, where h_f = h_m = ¼. The grey shaded regions show the expanded parameter space for balancing selection caused by the dominance reversal. This expanded parameter space due to dominance reversal is particularly pronounced when selection is modest to weak (right panel). Stronger dominance reversals (h_f and h_m < ¼) further expand the conditions for balancing selection. Theoretical curves are based on Eq 1, and the figure is based on Figs 1 and 3 of Kidwell and colleagues [9]. A_f, female-beneficial allele; A_m, male-beneficial allele; h_f, dominance coefficient of the A_m allele in females; h_m, dominance coefficient of the A_f allele in males; SA, sexually antagonistic; s_f, the cost to females of being homozygous for the A_m allele; s_m, the cost to males of being homozygous for the A_f allele.

Fig 2. Dominance emerges from concave fitness surfaces.

(A) Wright’s theory of dominance (based on Fig 7 from Wright [41] and Fig 1 from Otto and Bourguet [38]). A concave relation between gene activity and fitness causes deleterious mutations to be partially recessive to beneficial ones. In the example, a beneficial allele, A, and deleterious allele, a, have additive effects on gene activity (i.e., alleles alter gene transcription or function by amount Δx). The diminishing-return relation between fitness and gene activity results in partial recessivity of a with respect to fitness (h < ½). (B) Dominance reversal at an SA gene (based on Fig 1 from Gillespie and Langley [44] and Fig 2 from Fry [27]). The fitness surfaces for females and males (in blue and red, respectively) are each concave but have different optima. The SA alleles have additive effects on gene activity (i.e., by Δx); the concave mapping of fitness on gene activity causes the deleterious variant for each sex to be partially recessive (h_f and h_m < ½), so that A_f is partially recessive in males and A_m is partially recessive in females. A_m, male-beneficial allele; h_f, dominance coefficient of the A_m allele in females; h_m, dominance coefficient of the A_f allele in males; SA, sexually antagonistic.

Fig 3. Axes of SA and sexually concordant fitness variation.

The sexually concordant axis of genetic variation is marked in blue. The SA axis of genetic variation is marked in red. Circles show fitness estimates for a set of hypothetical experimental genotypes. SA, sexually antagonistic.