Large-Scale Trends in the Evolution of Gene Structures within 11 Animal Genomes

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Abstract
We have used the annotations of six animal genomes (Homo sapiens, Mus musculus, Ciona intestinalis, Drosophila melanogaster, Anopheles gambiae, and Caenorhabditis elegans) together with the sequences of five unannotated Drosophila genomes to survey changes in protein sequence and gene structure over a variety of timescales—from the less than 5 million years since the divergence of D. simulans and D. melanogaster to the more than 500 million years that have elapsed since the Cambrian explosion. To do so, we have developed a new open-source software library called CGL (for “Comparative Genomics Library”). Our results demonstrate that change in intron–exon structure is gradual, clock-like, and largely independent of coding-sequence evolution. This means that genome annotations can be used in new ways to inform, corroborate, and test conclusions drawn from comparative genomics analyses that are based upon protein and nucleotide sequence similarities. Just as protein sequences change over time, so do gene structures. Over comparatively short evolutionary timescales, introns lengthen and shorten; and over longer timescales the number and positions of introns in homologous genes can change. These facts suggest that the intron–exon structures of genes may provide a source of evolutionary information. The utility of gene structures as materials for phylogenetic analyses, however, depends upon their independence from the forces driving protein evolution. If, for example, intron–exon structures are strongly influenced by selection at the amino acid level, then using them for phylogenetic investigations is largely pointless, as the same information could have been more easily gained from protein analyses. Using 11 animal genomes, Yandell et al. show that evolution of intron lengths and positions is largely—though not completely—independent of protein sequence evolution. This means that gene structures provide a source of information about the evolutionary past independent of protein sequence similarities—a finding the authors employ to investigate the accuracy of the protein clock and to explore the utility of gene structures as a means to resolve deep phylogenetic relationships within the animals.