The diverse effects of phenotypic dominance on hybrid fitness

Abstract

When divergent populations interbreed, their alleles are brought together in hybrids. In the initial F1 cross, most divergent loci are heterozygous. Therefore, F1 fitness can be influenced by dominance effects that could not have been selected to function well together. We present a systematic study of these F1 dominance effects by introducing variable phenotypic dominance into Fisher's geometric model. We show that dominance often reduces hybrid fitness, which can generate optimal outbreeding followed by a steady decline in F1 fitness, as is often observed. We also show that "lucky" beneficial effects sometimes arise by chance, which might be important when hybrids can access novel environments. We then show that dominance can lead to violations of Haldane's Rule (reduced fitness of the heterogametic F1) but strengthens Darwin's Corollary (F1 fitness differences between cross directions).Taken together, results show that the effects of dominance on hybrid fitness can be surprisingly difficult to isolate, because they often resemble the effects of uniparental inheritance or expression. Nevertheless, we identify a pattern of environment-dependent heterosis that only dominance can explain, and for which there is some suggestive evidence. Our results also show how existing data set upper bounds on the size of dominance effects. These bounds could explain why additive models often provide good predictions for later-generation recombinant hybrids, even when dominance qualitatively changes outcomes for the F1.

How does the mode of evolutionary divergence affect reproductive isolation?

“…When there is phenotypic dominance (Lynch and Walsh, 1998, Ch. 4, Schneemann et al, 2022) we also need to account for the dominance deviations associated with allele frequency changes. We can do this by considering the mean phenotype in the initial F1 cross between P1 and P2, in which all loci in all individuals carry one P1-derived allele and one P2-derived allele.…”

“…the separate functions M (·, ·) and m (·, ·), are estimable under some conditions. This is clearest if the dominance effects are negligible (see Schneemann et al, 2022 for a discussion). In that case, all terms containing the Δ vanish, and the F1 trait means and variances are equal to the midparental values.…”

“…The n homozygous effects for each new mutation were drawn from a multivariate normal distribution with zero mean and no covariances, and a common variance set such that the mean deleterious effects of a mutation in an optimal background was . The heterozygous effect of each mutation on each trait was set at its homozygous effect multiplied by a beta-distributed random number, with bounds at 0 and 1 (corresponding to complete recessivity or complete dominance), a mean μ = 1 / 2 (implying additivity on average), and a variance of ν = 1 / 24 (Schneemann et al, 2022). After a total of D substitutions had fixed across both populations, the two parental genotypes were chosen as the genotypes containing only the fixed effects in each population.…”

“…. effects are not expressed together in the parental genotypes during the divergence process, and so unlike the additive effects, the dominance effects show little tendency to be coadapted to their optimum, but are free to wander in phenotypic space (Schneemann et al, 2020(Schneemann et al, , 2022.…”

“…In the latter case, the phenotypic model need not be treated literally, but is a simple way of generating a fitness landscape (Martin and Lenormand, 2006; Martin, 2014). Both uses of the model have been applied to hybrids (Lande, 1981; Mani and Clarke, 1990; Barton, 2001; Chevin et al, 2014; Fraïsse et al, 2016; Simon et al, 2018; Yamaguchi and Otto, 2020; Schneemann et al, 2020; Thompson et al, 2021; Schneemann et al, 2022).…”