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

Mol Biol Evol. 2008 Aug;25(8):1639-50. doi: 10.1093/molbev/msn111. Epub 2008 May 13.

Abstract

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, that is, 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 2 sexes. Using both single- and multilocus 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.

Publication types

  • Comparative Study
  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Adaptation, Biological / genetics*
  • Animals
  • Base Sequence
  • Drosophila / genetics*
  • Drosophila Proteins / genetics*
  • Drosophila Proteins / metabolism
  • Evolution, Molecular*
  • Female
  • Gene Expression*
  • Genes, X-Linked / genetics*
  • Male
  • Molecular Sequence Data
  • Polymorphism, Genetic*
  • Sequence Analysis, DNA
  • Sex Factors

Substances

  • Drosophila Proteins