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Open Access Highly Accessed Research article

A genome-wide survey of changes in protein evolutionary rates across four closely related species of Saccharomyces sensu stricto group

Yoshihiro Kawahara12 and Tadashi Imanishi1*

Author Affiliations

1 Integrated Database Group, Biological Information Research Center, National Institute of Advanced Industrial Science and Technology, 2-42 Aomi, Koto-ku, Tokyo 135-0064, Japan

2 Department of Biological Sciences, Tokyo Metropolitan University, 1-1 Minami-Osawa, Hachioji-shi, Tokyo 192-0397, Japan

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BMC Evolutionary Biology 2007, 7:9  doi:10.1186/1471-2148-7-9

Published: 29 January 2007



Changes in protein evolutionary rates among lineages have been frequently observed during periods of notable phenotypic evolution. It is also known that, following gene duplication and loss, the protein evolutionary rates of genes involved in such events changed because of changes in functional constraints acting on the genes. However, in the evolution of closely related species, excluding the aforementioned situations, the frequency of changes in protein evolutionary rates is still not clear at the genome-wide level. Here we examine the constancy of protein evolutionary rates in the evolution of four closely related species of the Saccharomyces sensu stricto group (S. cerevisiae, S. paradoxus, S. mikatae and S. bayanus).


For 2,610 unambiguously defined orthologous genes among the four species, we carried out likelihood ratio tests between constant-rate and variable-rate models and found 344 (13.2%) genes showing significant changes in the protein evolutionary rates in at least one lineage. Of all those genes which experienced rate changes, 139 and 49 genes showed accelerated and decelerated evolution, respectively. Most of the evolutionary rate changes could be attributed to changes in selective constraints acting on nonsynonymous sites, independently of species-specific gene duplication and loss. We estimated that the changes in protein evolutionary rates have appeared with a probability of 2.0 × 10-3 per gene per million years in the evolution of the Saccharomyces species. Furthermore, we found that the genes which experienced rate acceleration have lower expression levels and weaker codon usage bias than those which experienced rate deceleration.


Changes in protein evolutionary rates possibly occur frequently in the evolution of closely related Saccharomyces species. Selection for translational accuracy and efficiency may dominantly affect the variability of protein evolutionary rates.