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MBE Advance Access published online on June 6, 2006
Molecular Biology and Evolution, doi:10.1093/molbev/msl033
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© The Author 2006. 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
Accepted June 1, 2006

Research Article

Gene Regulation Divergence is a Major Contributor to the Evolution of Dobzhansky-Muller Incompatibilities between Species of Drosophila

Wilfried Haerty 1 and Rama S. Singh 1 *

1 Department of Biology, McMaster University, 1280 Main Street West, Hamilton, Ontario CANADA L8S 4K1

* To whom correspondence should be addressed.
Rama S. Singh, E-mail: singh{at}mcmaster.ca


  Abstract

The Dobzhansky-Muller model denotes incompatible gene interactions between diverging populations/species and is recognized as the basis of post-zygotic reproductive isolation. Little is known about the molecular nature of such gene interactions. We have carried out comparative gene expression analyses in the testes of three closely related species of the Drosophila melanogaster subgroup and their hybrids (all of which are sterile). We show that in hybrids: (i) a higher proportion of male-biased genes (i.e. genes with a higher level of expression in males) are under-expressed (or not expressed) compared to non-sex-biased genes, (ii) the majority of the under-expressed genes in hybrids appear to be under stabilizing selection by virtue of showing similar levels of expression in the parental species; only a small proportion of genes show signs of directional selection, (iii) very few of the misexpressed genes are shared between species-pairs suggesting that there may not be a common set of "speciation genes", and (iv) Expression of non-testes-specific genes is observed in the testes of interspecific hybrids, and the number of such genes is positively correlated with divergence time. These results suggest that gene regulation divergence of sex- and reproduction-related genes is a major contributor to the evolution of Dobzhansky-Muller incompatibilities between species of Drosophila.

Keywords: Gene regulation; Hybrid male sterility; stabilizing selection; sex-biased genes; Haldane's rule; Dobzhansky-Muller incompatibilities.
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