Gene regulatory divergence between locally adapted ecotypes in their native habitats

Local adaptation is a key driver of ecological specialization and the formation of new species. Despite its importance, the evolution of gene regulatory divergence among locally-adapted populations is poorly understood, especially how that divergence manifests in nature. Here, we evaluate gene expression divergence and allele-specific gene expression responses for locally-adapted coastal perennial and inland annual accessions of the yellow monkeyflower, Mimulus guttatus, in a field reciprocal transplant experiment. Overall, 6765 (73%) of surveyed genes were differentially expressed between coastal and inland habitats, while 7213 (77%) were differentially expressed between the coastal perennial and inland annual accessions. Further, 18% of transcripts had significant genotype x site (GxE) effects. Habitat-specific differential expression was found for 62% of the GxE transcripts (differential expression in one habitat, but not the other), while only 94 (~5%) GxE transcripts had crossing reaction norms. Cis-regulatory variation was pervasive, affecting 79% (5532) of differentially expressed genes. We detected trans effects for 52% (3611) of differentially expressed genes. Consistent with the supergene hypothesis of chromosome inversion evolution, a locally adaptive inversion was enriched for cis-regulatory divergence. Above and below mid-parent heterosis for gene expression was prevalent across habitats and heterotic genes were enriched for growth and development gene ontologies. These results provide multiple new insights into the evolution of transcriptome-wide gene regulatory divergence and plasticity among locally adapted populations.