Dominance reversal of inversion karyotypes - RNAseq

How genetic variance for fitness is maintained is incompletely understood. Mutation-selection balance and single-locus overdominance cannot account for the large amount of variance observed. Recent work suggests that antagonistic selection, favoring different alleles in different contexts and involving beneficial dominance reversals, might contribute to maintaining fitness variance. However, while this mechanism is plausible, evidence for dominance reversals is scarce. Here, we study how In(3R)Payne, a D. melanogaster inversion polymorphism maintained by balancing selection, affects gene expression and chromatin accessibility. Using RNA-seq and ATAC-seq, we find that in embryos the inverted (INV) arrangement tends to have dominant effects on expression, with the standard (STD) arrangement behaving like a recessive Mendelian allele. Yet, in wing discs, this pattern is reversed: STD has mostly dominant effects, whereas INV tends to behave recessively. Since this dominance reversal between developmental contexts affects the expression of suites of genes in a concerted manner, it might be mediated by a dominance modifier, for example a transcription factor, as recently postulated theoretically. In favor of this idea, 25% of the differentially expressed genes between INV and STD encode transcription factors. Interestingly, while only four differentially expressed genes are shared between embryos and wing discs, one of them is HP1c, a chromatin binding protein and major transcriptional regulator, and thus a promising candidate for mediating the context-dependent dominance reversal. Although the relation between these patterns and fitness is presently unknown, our observations are consistent with a potential role of dominance reversals in maintaining inversion polymorphism.