Strength of stabilizing selection is associated with the amount of non-additive variance in gene expression

The distinction between the additive (inherited) and non-additive components of genetic variance is crucial for predicting the adaptive potential of a trait. Yet we know surprisingly little about the genomic and evolutionary factors that influence non-additive genetic variance in natural populations. Here, we use a quantitative genetic breeding design to decompose the additive and non-additive components of variance of 17,657 gene transcripts in the outcrossing plant Arabidopsis lyrata. We find that the major fraction of gene expression variance in our data corresponds to non-additive variance. Transcripts showing the highest levels of non-additive variance tend to be longer, cluster in larger groups of co-expressed genes, and are particularly enriched among genes involved in cellular differentiation and epigenetic reprogramming of gene expression. Furthermore, we find that genes with the highest fraction of non-additive variation are exposed to stronger stabilizing selection than genes with higher additive variance. As a source of many evolutionary novelties, gene expression variation plays a key role in adaptive evolution, yet only additive genetic variation is inherited and can therefore respond to selection. Our study indicates that stabilizing selection has eroded additive genetic variation and the remaining non-additive variation does not contribute to short-term adaptation .