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Ribosomal proteins are essential to life. While the functions of ribosomal protein-encoding genes (RPGs) are highly conserved, the evolution of their regulatory mechanisms is remarkably dynamic. In  Saccharomyces cerevisiae , RPGs are unusual in that they are commonly present as two highly similar gene copies and in that they are over-represented among intron-containing genes. To investigate the role of introns in the regulation of RPG expression, we constructed 16  S. cerevisiae  strains with precise deletions of RPG introns. We found that several yeast introns function to repress rather than to increase steady-state mRNA levels. Among these, the  RPS9A  and  RPS9B  introns were required for cross-regulation of the two paralogous gene copies, which is consistent with the duplication of an autoregulatory circuit. To test for similar intron function in animals, we performed an experimental test and comparative analyses for autoregulation among distantly related animal  RPS9  orthologs. Overexpression of an exogenous  RpS9  copy in  Drosophila melanogaster  S2 cells induced alternative splicing and degradation of the endogenous copy by nonsense-mediated decay (NMD). Also, analysis of expressed sequence tag data from distantly related animals, including  Homo sapiens  and  Ciona intestinalis , revealed diverse alternatively-spliced  RPS9  isoforms predicted to elicit NMD. We propose that multiple forms of splicing regulation among  RPS9  orthologs from various eukaryotes operate analogously to translational repression of the alpha operon by S4, the distant prokaryotic ortholog. Thus,  RPS9  orthologs appear to have independently evolved variations on a fundamental autoregulatory circuit.

Diverse Forms of RPS9 Splicing Are Part of an Evolving Autoregulatory Circuit