MBE Advance Access published online on February 23, 2008
Molecular Biology and Evolution, doi:10.1093/molbev/msn055
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Research Article |
Evolution of Gene Expression in the Drosophila Olfactory System
1 Section of Evolution and Ecology, University of California – Davis, Davis CA 95616
2 Department of Biology, Indiana University, Bloomington IN 47405
3 NASA Ames Research Center, Moffett Field, CA 94035
4 University of Florida Genetics Institute, University of Florida, Gainesville FL 32611
5 Department of Molecular Genetics and Microbiology, University of Florida, Gainesville FL 32611
6 Department of Biology and Carolina Center for Genome Science, University of North Carolina – Chapel Hill, Chapel Hill NC 27599
* Author for correspondence: Section of Evolution and Ecology, University of California – Davis, One Shields Ave, Davis, CA 95161, phone (530) 752-8657, fax (530) 752-9014, akopp{at}ucdavis.edu
Received for publication November 21, 2007. Revision received February 9, 2008. Accepted for publication February 15, 2008.
Host plant shifts by phytophagous insects play a key role in insect evolution and plant ecology. Such shifts often involve major behavioral changes, as the insects must acquire an attraction and/or lose the repulsion to the new host plant's odor and taste. The evolution of chemotactic behavior may be due, in part, to gene expression changes in the peripheral sensory system. To test this hypothesis, we compared gene expression in the olfactory organs of Drosophila sechellia, a narrow ecological specialist that feeds on the fruit of Morinda citrifolia, to its close relatives D. simulans and D. melanogaster, which feed on a wide variety of decaying plant matter. Using whole-genome microarrays and quantitative PCR, we surveyed the entire repertoire of Drosophila odorant receptors (ORs) and odorant binding proteins (OBPs) expressed in the antennae. We found that the evolution of OR and OBP expression was accelerated in D. sechellia compared both to the genome average in that species and to the rate of OR and OBP evolution in the other species. However, some of the gene expression changes that correlate with D. sechellia's increased sensitivity to Morinda odorants may pre-date its divergence from D. simulans. Interspecific divergence of olfactory gene expression cannot be fully explained by changes in the relative abundance of different sensilla, as some ORs and OBPs have evolved independently of other genes expressed in the same sensilla. A number of OR and OBP genes are upregulated in D. sechellia compared to its generalist relatives. These genes include Or22a, which likely responds to a key odorant of M. citrifolia, and several genes that are yet to be characterized in detail. Increased expression of these genes in D. sechellia may have contributed to the evolution of its unique chemotactic behavior.
Key Words: olfactory receptors • Drosophila sechellia • gene expression • microarrays • regulatory evolution • host plant preferences