Gene expression evolution is predicted by stronger indirect selection at more pleiotropic genes.

Area of Science:

• Evolutionary Biology
• Genomics
• Molecular Biology

Background:

• Gene expression changes are crucial for adaptation, but predicting their evolutionary trajectory is difficult.
• Understanding the mechanisms driving adaptive evolution at the gene expression level is a key challenge.

Purpose of the Study:

• To identify genes under selection for expression changes during adaptation to heat and drought stress in *Tribolium castaneum*.
• To uncover the mechanisms driving adaptive evolution of gene expression.
• To assess the predictive power of transcriptome-wide selection estimates for evolutionary changes.

Main Methods:

• Transcriptome-wide analysis of gene expression variation in *Tribolium castaneum*.
• Experimental evolution under heat and drought stress across multiple independent selection lines.
• Genomic analysis of allele frequency changes and their correlation with expression selection.

Main Results:

• Genetic selection estimates on expression levels accurately predicted evolutionary changes after 20 generations.
• Evolution of gene expression was primarily driven by indirect selection on genetically correlated genes, not direct selection on single genes.
• Central genes within co-expression networks exhibited stronger selection and greater expression changes, contrary to previous hypotheses.
• Selection on expression levels correlated with parallel allele frequency changes, especially in pleiotropic genes and those with expression quantitative trait loci.

Conclusions:

• Transcriptome-level selection measurements can predict future gene expression evolution.
• Adaptation is facilitated by selection acting on gene networks, particularly central genes, providing mechanistic insights into the genetic basis of adaptation.
• The study highlights the importance of indirect selection and network architecture in shaping adaptive evolution.