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Originally published as Genetics Published Articles Ahead of Print on September 2, 2005.
Genetics, Vol. 171, 1813-1822, December 2005, Copyright © 2005
doi:10.1534/genetics.105.047449
Compensatory cis-trans Evolution and the Dysregulation of Gene Expression in Interspecific Hybrids of Drosophila
Christian R. Landry*,
Patricia J. Wittkopp
,
Clifford H. Taubes
,
Jose M. Ranz
,
Andrew G. Clark and
Daniel L. Hartl*,1
* Department of Organismic and Evolutionary Biology and Department of Mathematics, Harvard University, Cambridge, Massachusettts 02138, Department of Molecular Biology and Genetics, Cornell University, Ithaca, New York 14853 and Department of Genetics, University of Cambridge, Cambridge CB2 3EH, United Kingdom
1 Corresponding author: Department of Organismic and Evolutionary Biology, The Biological Laboratories, 16 Divinity Ave., Cambridge, MA 02138.
E-mail: dhartl{at}oeb.harvard.edu
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.
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