Evolutionary trade-off and mutational bias could favor transcriptional over translational divergence within paralog pairs

How changes in the different steps of protein synthesis-transcription, translation and degradation-contribute to differences of protein abundance among genes is not fully understood. There is however accumulating evidence that transcriptional divergence might have a prominent role. Here, we show that yeast paralogous genes are more divergent in transcription than in translation. We explore two causal mechanisms for this predominance of transcriptional divergence: an evolutionary trade-off between the precision and economy of gene expression and a larger mutational target size for transcription. Performing simulations within a minimal model of post-duplication evolution, we find that both mechanisms are consistent with the observed divergence patterns. We also investigate how additional properties of the effects of mutations on gene expression, such as their asymmetry and correlation across levels of regulation, can shape the evolution of paralogs. Our results highlight the importance of fully characterizing the distributions of mutational effects on transcription and translation. They also show how general trade-offs in cellular processes and mutation bias can have far-reaching evolutionary impacts. Author summaryChanges in the cellular abundance of proteins are of great importance in evolution, as they are associated with phenotypic variation and adaptation. They can result from mutations acting on multiple biochemical processes, of which the most important are the transcription of mRNAs and their translation into polypeptides. While the evolution of transcription levels has been extensively studied, the interplay between transcriptional and translational changes remains to be fully elucidated. Yet, there is accumulating evidence that transcription may evolve at a faster rate. We show that this is the case within paralog pairs of the yeast Saccharomyces cerevisiae, where divergence is significantly larger at the transcriptional level than at the translational one. Using simulations, we compare two potential mechanisms by which such patterns could arise: an evolutionary trade-off in the process of protein synthesis and a higher probability-or larger effects-for mutations affecting transcription. We find that both explanations are consistent with the observed divergence of duplicated genes. Whether these apply generally to all genes or exclusively to paralogs, this work still provides important insights on the evolution of gene expression levels. Gene duplication events indeed occur frequently and are thus likely to have profound and lasting impacts on the evolution of protein abundance levels.

Automated summary

The contribution of changes in transcription, translation, and degradation to the differences in protein abundance among genes is not fully understood. This study reveals that transcriptional divergence is more prominent than translational divergence in yeast paralogous genes and identifies two potential mechanisms for this pattern: an evolutionary trade-off between gene expression precision and economy, and a larger mutational target size for transcription. Simulations using a minimal model of post-duplication evolution support both mechanisms. These findings emphasize the importance of characterizing mutational effects on transcription and translation and highlight the evolutionary impacts of cellular trade-offs and mutation bias.