Dominance reversals: the resolution of genetic conflict and maintenance of genetic variation

Abstract

Beneficial reversals of dominance reduce the costs of genetic trade-offs and can enable selection to maintain genetic variation for fitness. Beneficial dominance reversals are characterized by the beneficial allele for a given context (e.g. habitat, developmental stage, trait or sex) being dominant in that context but recessive where deleterious. This context dependence at least partially mitigates the fitness consequence of heterozygotes carrying one non-beneficial allele for their context and can result in balancing selection that maintains alternative alleles. Dominance reversals are theoretically plausible and are supported by mounting empirical evidence. Here, we highlight the importance of beneficial dominance reversals as a mechanism for the mitigation of genetic conflict and review the theory and empirical evidence for them. We identify some areas in need of further research and development and outline three methods that could facilitate the identification of antagonistic genetic variation (dominance ordination, allele-specific expression and allele-specific ATAC-Seq (assay for transposase-accessible chromatin with sequencing)). There is ample scope for the development of new empirical methods as well as reanalysis of existing data through the lens of dominance reversals. A greater focus on this topic will expand our understanding of the mechanisms that resolve genetic conflict and whether they maintain genetic variation.

Keywords: antagonistic pleiotropy; balancing selection; dominance reversal; genetic conflict; genetic trade-offs; genetic variation.

Figure 1.

Graphical representation of beneficial dominance reversals. Circles versus triangles represent alternative sexes, environments or generations (antagonistic pleiotropy scenarios not shown). We first map genotype to trait expression under two scenarios: (a) additivity for the phenotype, and (b) dominance reversal for the phenotype. Then we map trait expression to fitness under two scenarios of antagonistic selection: (c) additivity for fitness and (d) curved fitness functions overlapping in their concave vicinities. The ultimate effect of a genotype on fitness is given by the combination of the genotype-phenotype map (a or b) and the phenotype-fitness map (c or d) in the matrix of resultant genotype-fitness panels (i–iv): (i) additivity, (ii) dominance reversal owing to the genotype-phenotype map or (iii) owing to the phenotype-fitness map, and (iv) a greater magnitude of dominance reversal owing to their combined effects. See electronic supplementary material, figure S1 for varying parameter settings, convex fitness functions, heterozygote inferiority, etc.