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MBE Advance Access published online on September 19, 2007

Molecular Biology and Evolution, doi:10.1093/molbev/msm199
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© The Author 2007. 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

Adaptive Protein Evolution of X-Linked and Autosomal Genes in Drosophila: Implications for Faster-X Hypotheses

Tim Connallon

Department of Ecology and Evolutionary Biology and Museum of Zoology, University of Michigan, Ann Arbor, MI 48109-1048

Corresponding author: Tim Connallon, University of Michigan, Museum of Zoology (Insect Division), 1109 Geddes Ave. Ann Arbor, MI 48109-1079, Phone: (734) 763-7943, Fax: (734) 763-4080, Email: tconnal{at}umich.edu

Received for publication June 11, 2007. Revision received September 6, 2007. Accepted for publication September 12, 2007.

Patterns of sex chromosome and autosome evolution can be used to elucidate the underlying genetic basis of adaptative change. Evolutionary theory predicts that X-linked genes will adapt more rapidly than autosomes if adaptation is limited by the availability of beneficial mutations, and if such mutations are recessive. In Drosophila, rates of molecular divergence between species appear to be equivalent between autosomes and the X chromosome. However, molecular divergence contrasts are difficult to interpret because they reflect a composite of adaptive and nonadaptive substitutions between species. Predictions based on faster-X theory also assume that selection is equally effective on the X and autosomes; this might not be true because the effective population sizes of X-linked and autosomal genes systematically differ. Here, population genetic and divergence data from Drosophila melanogaster, D. simulans and D. yakuba are used to estimate the proportion of adaptive amino acid substitutions occurring in the D. melanogaster lineage. After gene composition and effective population size differences between chromosomes are controlled, X-linked and autosomal genes are shown to have equivalent rates of adaptive divergence, with approximately 30 % of amino acid substitutions driven by positive selection. The results suggest that adaptation is either unconstrained by a lack of beneficial genetic variation, or that beneficial mutations are not recessive and are thus highly visible to natural selection whether on sex chromosomes or on autosomes.

Key Words: X chromosome • sex linkage • adaptive evolution • Hill-Robertson interference • effective population size • codon bias


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