Dominance, Epistasis and the Genetics of Postzygotic Isolation

TLDR

Hybrid sterility and inviability arise from Dobzhansky–Muller incompatibilities, which are common in Drosophila crosses and may explain exceptions to Haldane’s rule. The authors develop a two‑locus incompatibility model distinguishing H0, H1, and H2 interactions to investigate Haldane’s rule and the large effect of X chromosomes on postzygotic isolation. They predict hybrid fitness by computing expected numbers of H0, H1, and H2 incompatibilities and extend the model to include Y/W chromosome and maternal effects. The study shows that the relative severity of H0 versus H1 incompatibilities explains Haldane’s rule, while H1 versus H2 severity must also be considered for large X effects, which are not inevitable in backcrosses but often reflect recessive isolation alleles.

Abstract

Abstract The sterility and inviability of species hybrids can be explained by between-locus “Dobzhansky-Muller” incompatibilities: alleles that are fit on their “normal” genetic backgrounds sometimes lower fitness when brought together in hybrids. We present a model of two-locus incompatibilities that distinguishes among three types of hybrid interactions: those between heterozygous loci (H0), those between a heterozygous and a homozygous (or hemizygous) locus (H1), and those between homozygous loci (H2). We predict the relative fitnesses of hybrid genotypes by calculating the expected numbers of each type of incompatibility. We use this model to study Haldane's rule and the large effect of X chromosomes on postzygotic isolation. We show that the severity of H0 vs. H1 incompatibilities is key to understanding Haldane's rule, while the severity of H1 vs. H2 incompatibilities must also be considered to explain large X effects. Large X effects are not inevitable in backcross analyses but rather—like Haldane's rule—may often reflect the recessivity of alleles causing postzygotic isolation. We also consider incompatibilities involving the Y (or W) chromosome and maternal effects. Such incompatibilities are common in Drosophila species crosses, and their consequences in male- vs. female-heterogametic taxa may explain the pattern of exceptions to Haldane's rule.