MBE Advance Access published online on July 28, 2003
Molecular Biology and Evolution, doi:10.1093/molbev/msg178
Molecular Biology and Evolution © Society for Molecular Biology and Evolution 2003; all rights reserved
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1 Department of Human Genetics, Howard Hughes Medical Institute, University of Chicago, Chicago, IL 60637, USA; Department of Anthropology, Howard Hughes Medical Institute, University of Chicago, Chicago, IL 60637, USA
* To whom correspondence should be addressed. E-mail: wyckoffg{at}umkc.edu.
The reduction of mutation rates on the mammalian X chromosome relative to autosomes is most often explained in the literature as evidence of male-driven evolution. This hypothesis attributes lowered mutation rates on the X to the fact that this chromosome spends less time in the germ line of males than females. In contrast to this majority view, two articles argued that the patterns of mutation rates across chromosomes are inconsistent with male-driven evolution. McVean and Hurst (1997) reported a 40% reduction in synonymous substitution rates (Ks) for X-linked genes relative to autosomes in the mouse-rat lineage. They argued that this reduction is too dramatic to be explained by male-driven evolution, and concluded that selection has systematically reduced mutation rate on the X to a level optimal for this male-hemizygous chromosome. More recently, Lercher et al. (2001) found that chromosomal mutation rates in both the human-mouse and mouse-rat lineages were so heterogeneous that the X was not an outlier. Here again, the authors argued that this is at odds with male-driven evolution and suggested that selection has modulated chromosomal mutation rates to locally optimal levels, thus extending the argument of McVean and Hurst (1997) to include autosomes. Here, we reexamine these conclusions using mouse-rat and human-mouse coding-region data. We find a more modest reduction of Ks on the X chromosome than did McVean and Hurst (1997), but our results contradict the finding of Lercher et al. (2001) that the X chromosome is not distinct from autosomes. Multiple statistical tests show that Ks rates on the X differ systematically from the autosomes in both lineages. We conclude that the moderate yet consistent reduction of mutation rate on the X chromosome of both lineages is consistent with male-driven evolution; however, the large variance in mutation rates across chromosomes suggests that mutation rates are affected by additional factors besides male-driven evolution. Investigation of mutation rates by synteny reveals that synteny blocks, rather than entire chromosomes as suggested by Lercher et al. (2001), might represent the unit of mutation rate variation. Key Words:
comparative genomics, male-driven evolution, mutation rate, molecular evolution, sex chromosomes, synteny bins
© 2003 Society for Molecular Biology and Evolution
Original Articles
Genic Mutation Rates in Mammals: Local Similarity, Chromosomal Heterogeneity, and X-Versus-Autosome Disparity
2 Department of Human Genetics, Howard Hughes Medical Institute, University of Chicago, Chicago, IL 60637, USA
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