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MBE Advance Access published online on April 11, 2008
Molecular Biology and Evolution, doi:10.1093/molbev/msn089
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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

Recurrent Tandem Gene Duplication Gave Rise to Functionally Divergent Genes in Drosophila

Chuanzhu Fan*,1, Ying Chen{boxvh},2 and Manyuan Long*,{boxvh}

* Department of Ecology and Evolution and
{boxvh} the Committee on Genetics, The University of Chicago, Chicago, IL 60637, USA

Corresponding authors: Chuanzhu Fan, Arizona Genomics Institute, Department of Plant Sciences, University of Arizona, Tucson, AZ 85721. Tel: 520-626-9594; Fax: 520-621-1259; email: cfan{at}cals.arizona.edu. Manyuan Long, Department of Ecology and Evolution, The University of Chicago, 1101 E 57th St., Chicago, IL 60637, USA; Tel: 773-702-0557; fax: 773-702-9740; email: mlong{at}uchicago.edu.

Received for publication December 12, 2007. Revision received February 15, 2008. Revision received March 24, 2008. Accepted for publication April 7, 2008.

Tandem gene duplication is one of the major gene duplication mechanisms in eukaryotes, as illustrated by the prevalence of gene family clusters. Tandem duplicated paralogs usually share the same regulatory element and as a consequence they are likely to perform similar biological functions. Here, we provide an example of a newly evolved tandem duplicate acquiring novel functions that were driven by positive selection. CG32708, CG32706, and CG6999 are three clustered genes residing in the X chromosome of D. melanogaster. CG6999 and CG32708 have been examined for their molecular population genetic properties (Thornton and Long, 2005). We further investigated the evolutionary forces acting on these genes with greater sample sizes and a broader approach that incorporate between-species divergence, using more variety of statistical methods. We explored the possible functional implications by characterizing the tissue-specific and developmental expression patterns of these genes. Sequence comparison of species within D. melanogaster subgroup reveals that this three gene cluster was created by two rounds of tandem gene duplication in the last 5 million years (my). Based on phylogenetic analysis, CG32708 is clearly the parental copy that is shared by all species. CG32706 appears to have originated in the ancestor of D. simulans and D. melanogaster about 5 million years ago (mya) and CG6999 is the newest duplicate that is unique to D. melanogaster. All three genes have different expression profiles, and CG6999 has in addition acquired a novel transcript. Biased polymorphism frequency spectrum, linkage disequilibrium (LD), nucleotide substitution, and McDonald-Kreitman (MK) analyses suggested that the evolution of CG6999 and CG32706 were driven by positive Darwinian selection.

Key Words: Drosophila • Positive selection • Tandem duplication • Young gene

1 Present address: Arizona Genomics Institute, Department of Plant Sciences, University of Arizona, Tucson, AZ 85721.

2 Present address: Department of Biology, University College London, Darwin Building, Gower Street, London WC1E 6BT, UK.


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