Genetics. Published Articles Ahead of Print: September 2, 2005, Copyright © 2005
doi:10.1534/genetics.105.047449


A more recent version of this article appeared on December 1, 2005.


REGULAR RESEARCH PAPERS

Compensatory cis-trans Evolution and the Dysregulation of Gene Expression in Interspecific Hybrids of Drosophila

1 Harvard University
2 Cornell University
3 University of Cambridge

* To whom correspondence should be addressed. E-mail: dhartl{at}oeb.harvard.edu.

Submitted on June 29, 2005
Revised on August 12, 2005
Accepted on 25 August 2005


Abstract

Hybrids between species are often characterized by novel gene-expression patterns. A recent study on allele-specific gene expression in hybrids between species of Drosophila revealed cases in which cis and trans regulatory elements within species had coevolved in such a way that changes in cis-regulatory elements are compensated by changes in trans-regulatory elements. We hypothesized that such coevolution should often lead to gene misexpression in the hybrid. To test this hypothesis, we estimated allele-specific expression and overall expression levels for 31 genes in D. melanogaster, D. simulans, and their F1 hybrid. We found that 13 genes with cis-trans compensatory evolution are in fact misexpressed in the hybrid. These represent candidate genes whose dysregulation might be the consequence of coevolution of cis and trans regulatory elements within species. Using a mathematical model for the regulation of gene expression, we explored the conditions under which cis-trans compensatory evolution can lead to misexpression in interspecific hybrids.

Key Words: Drosophila, Gene regulation, allele-specific expression, dysregulation, interspecific hybrids




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