Gene expression levels correlate with multiple aspects of gene sequence and gene structure in phylogenetically diverse taxa suggesting an important role of gene expression levels in the evolution of protein-coding genes. Here we present results of a genome-wide study of the influence of gene expression on synonymous codon usage, amino acid composition and gene structure in the red flour beetle, Tribolium castaneum. Consistent with the action of translational selection, we find that synonymous codon usage bias increases with gene expression. However, the correspondence between tRNA gene copy number and optimal codons is weak. At the amino acid level, translational selection is suggested by the positive correlation between tRNA gene numbers and amino acid usage which is stronger for highly expressed genes. In addition, there is a clear trend for increased use of metabolically cheaper, less complex, amino acids as gene expression increases. tRNA gene numbers also correlate negatively with amino acid size/complexity score indicating the coupling between translational selection and selection to minimize the use of large/complex amino acids. Interestingly, the correlation between tRNA gene numbers and amino acid size/complexity score appears to be widespread given our analyses of 10 additional genomes and might be explained by selection against negative consequences of protein misfolding. At the level of gene structure, three major trends are detected 1) CDS length increases across low and intermediate expression levels but decreases in highly expressed genes; 2) the average intron size shows the opposite trend, first decreasing with expression, followed by a slight increase in highly expressed genes and 3) intron density remains nearly constant across all expression levels. These changes in gene architecture are only in partial agreement with selection favoring reduced cost of biosynthesis.