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Genome Biology and Evolution Advance Access originally published online on July 7, 2009
Genome Biology and Evolution (2009) Vol. 2009:176; doi:10.1093/gbe/evp018 published on July 31, 2009
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© 2009 The Authors
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.0/uk/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

A Complex Suite of Forces Drives Gene Traffic from Drosophila X Chromosomes

Richard P. Meisel*,{dagger}, Mira V. Han{ddagger} and Matthew W. Hahn{ddagger},§

* Department of Biology and Graduate Program in Genetics, The Pennsylvania State University
{dagger} Department of Molecular Biology and Evolution, Cornell University
{ddagger} School of Informatics, Indiana University
§ Department of Biology, Indiana University

E-mail: rpm16{at}cornell.edu.


  Abstract

Theoretical studies predict X chromosomes and autosomes should be under different selection pressures, and there should therefore be differences in sex-specific and sexually antagonistic gene content between the X and the autosomes. Previous analyses have identified an excess of genes duplicated by retrotransposition from the X chromosome in Drosophila melanogaster. A number of hypotheses may explain this pattern, including mutational bias, escape from X-inactivation during spermatogenesis, and the movement of male-favored (sexually antagonistic) genes from a chromosome that is predominantly carried by females. To distinguish among these processes and to examine the generality of these patterns, we identified duplicated genes in nine sequenced Drosophila genomes. We find that, as in D. melanogaster, there is an excess of genes duplicated from the X chromosome across the genus Drosophila. This excess duplication is due almost completely to genes duplicated by retrotransposition, with little to no excess from the X among genes duplicated via DNA intermediates. The only exception to this pattern appears within the burst of duplication that followed the creation of the Drosophila pseudoobscura neo-X chromosome. Additionally, we examined genes relocated among chromosomal arms (i.e., genes duplicated to new locations coupled with the loss of the copy in the ancestral locus) and found an excess of genes relocated off the ancestral X and neo-X chromosomes. Interestingly, many of the same genes were duplicated or relocated from the independently derived neo-X chromosomes of D. pseudoobscura and Drosophila willistoni, suggesting that natural selection favors the traffic of genes from X chromosomes. Overall, we find that the forces driving gene duplication from X chromosomes are dependent on the lineage in question, the molecular mechanism of duplication considered, the preservation of the ancestral copy, and the age of the X chromosome.

Keywords: gene duplication, retrotransposition, sex chromosomes, neo-X chromosomes, X-inactivation

Accepted July 3, 2009

Chung-I Wu, Associate Editor


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