Different and contrasting models have been proposed to explain intron size evolution in mammals. Here, we demonstrate that intron and intergenic size per se has no adaptive role in gene expression regulation but reflects the need to preserve conserved intronic elements. Although the amount of non-coding functional elements explains the within-genome size variation of intergenic spacers, we show that an additional, additive pressure has been acting on highly expressed introns to reduce the cost of their transcription.