Gene expression evolution during adaptation is predicted by stronger genetic selection at more pleiotropic genes in Tribolium castaneum

Changes in gene expression play a fundamental role in the process of adaptation and can inform on the genetic basis of adaptation. We utilized transcriptome-wide variation in gene expression as a means to uncover genes under selection for expression changes during adaptation to heat and drought stress and to understand the nature of selection on gene expression traits of the red flour beetle Tribolium castaneum . We showed that estimates of genetic selection on transcript abundance were predictive of evolutionary changes in gene expression after 20 generations of adaptation in seven independent experimental lines. Having measured the genetic covariance between gene expression and relative fitness and among expression traits, we showed that evolutionary changes were caused by indirect selection acting on genetically correlated partners rather than direct selection acting on isolated genes. Consequently, pleiotropic genes with central positions in gene co-expression networks experienced stronger selection and exhibited larger evolutionary changes in expression. Our genomic analysis revealed that selection on expression levels drives parallel allele frequency changes (AFC) in the respective genes. More pleiotropic genes and those carrying expression quantitative trait loci (eQTLs) showed a higher degree of parallel evolution. More generally, genes with more parallel AFCs were under stronger genetic selection. Contrary to previous evidence of constrained evolution at more connected genes, adaptation was driven by selection acting disproportionately on genes central to co-expression gene networks. We demonstrated that measures of selection at the transcriptome level can provide accurate evolutionary predictions and critical information on the molecular basis of rapid adaptation.