Codon Usage Differences among Genes Expressed in Different Tissues of Drosophila melanogaster

Codon usage patterns are affected by both mutational biases and translational selection. The frequency at which each codon is used in the genome is directly linked to the cellular concentrations of their corresponding tRNAs. Transfer RNA abundances—as well as the abundances of other potentially relevant factors, such as RNA-binding proteins—may vary across different tissues, making it possible that genes expressed in different tissues are subject to different translational selection regimes, and thus differ in their patterns of codon usage. These differences, however, are poorly understood, having been studied only in Arabidopsis, rice and human, with controversial results in human. Drosophila melanogaster is a suitable model organism to study tissue-specific codon adaptation given its large effective population size. Here, we compare 2,046 genes, each expressed specifically in one tissue of D. melanogaster. We show that genes expressed in different tissues exhibit significant differences in their patterns of codon usage, and that these differences are only partially due to differences in GC content, expression levels, or protein lengths. Remarkably, these differences are stronger when analyses are restricted to highly expressed genes. Our results strongly suggest that genes expressed in different tissues are subject to different regimes of translational selection.