Predominance of <i>cis</i>-regulatory changes in parallel expression divergence of sticklebacks.

Abstract

Regulation of gene expression is thought to play a major role in adaptation, but the relative importance of <i>cis</i>- and <i>trans</i>- regulatory mechanisms in the early stages of adaptive divergence is unclear. Using RNAseq of threespine stickleback fish gill tissue from four independent marine-freshwater ecotype pairs and their F1 hybrids, we show that <i>cis</i>-acting (allele-specific) regulation consistently predominates gene expression divergence. Genes showing parallel marine-freshwater expression divergence are found near to adaptive genomic regions, show signatures of natural selection around their transcription start sites and are enriched for <i>cis-</i>regulatory control. For genes with parallel increased expression among freshwater fish, the quantitative degree of <i>cis-</i> and <i>trans-</i>regulation is also highly correlated across populations, suggesting a shared genetic basis. Compared to other forms of regulation, <i>cis-</i>regulation tends to show greater additivity and stability across different genetic and environmental contexts, making it a fertile substrate for the early stages of adaptive evolution.