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MBE Advance Access published online on May 13, 2008
Molecular Biology and Evolution, doi:10.1093/molbev/msn111
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© The Author 2008. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org

Research Article

Effects of X-linkage and sex-biased gene expression on the rate of adaptive protein evolution in Drosophila

John F. Baines1, Stanley A. Sawyer2, Daniel L. Hartl3 and John Parsch1

1 Section of Evolutionary Biology, Department of Biology, University of Munich, 82152 Munich, Germany
2 Department of Mathematics, Washington University, St. Louis, MO 63130
3 Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138

Corresponding author: John Parsch, Department of Biology, University of Munich, Grosshaderner Str. 2, 82152 Planegg-Martinsried, Germany. Email: parsch{at}zi.biologie.uni-muenchen.de. Phone: +49 89 2170 74 107, Fax: +49 89 2170 74 104

Received for publication December 27, 2007. Revision received May 7, 2008. Accepted for publication May 7, 2008.

Patterns of polymorphism and divergence in Drosophila protein-coding genes suggest that a considerable fraction of amino acid differences between species can be attributed to positive selection and that genes with sex-biased expression, i.e. those expressed predominantly in one sex, have especially high rates of adaptive evolution. Previous studies, however, have been restricted to autosomal sex-biased genes and, thus, do not provide a complete picture of the evolutionary forces acting on sex-biased genes across the genome. To determine the effects of X-linkage on sex-biased gene evolution, we surveyed DNA sequence polymorphism and divergence in 45 X-linked genes, including 17 with male-biased expression, 13 with female-biased expression, and 15 with equal expression in the two sexes. Using both single- and multi-locus tests for selection, we found evidence for adaptive evolution in both groups of sex-biased genes. The signal of adaptive evolution was particularly strong for X-linked male-biased genes. A comparison with data from 91 autosomal genes revealed a "fast-X" effect, in which the rate of adaptive evolution was greater for X-linked than for autosomal genes. This effect was strongest for male-biased genes, but could be seen in the other groups as well. A genome-wide analysis of coding sequence divergence that accounted for sex-biased expression also uncovered a fast-X effect for male-biased and unbiased genes, suggesting that recessive beneficial mutations play an important role in adaptation.

Key Words: positive selection • gene expression • sex linkage • fast-X effect • Drosophila


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