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Genetics, Vol. 177, 1395-1416, November 2007, Copyright © 2007
doi:10.1534/genetics.107.078683
Five Drosophila Genomes Reveal Nonneutral Evolution and the Signature of Host Specialization in the Chemoreceptor Superfamily
Carolyn S. McBride*,1 and
J. Roman Arguello
,1,2
* Center for Population Biology, University of California, Davis, California 95616 and Committee on Evolutionary Biology, University of Chicago, Chicago, Illinois 60637
2 Corresponding author: Department of Ecology and Evolution, 1101 E. 57th St., Chicago, IL 60637. E-mail: arguello{at}uchicago.edu
The insect chemoreceptor superfamily comprises the olfactory receptor (Or) and gustatory receptor (Gr) multigene families. These families give insects the ability to smell and taste chemicals in the environment and are thus rich resources for linking molecular evolutionary and ecological processes. Although dramatic differences in family size among distant species and high divergence among paralogs have led to the belief that the two families evolve rapidly, a lack of evolutionary data over short time scales has frustrated efforts to identify the major forces shaping this evolution. Here, we investigate patterns of gene loss/gain, divergence, and polymorphism in the entire repertoire of 
130 chemoreceptor genes from five closely related species of Drosophila that share a common ancestor within the past 12 million years. We demonstrate that the overall evolution of the Or and Gr families is nonneutral. We also show that selection regimes differ both between the two families as wholes and within each family among groups of genes with varying functions, patterns of expression, and phylogenetic histories. Finally, we find that the independent evolution of host specialization in Drosophila sechellia and D. erecta is associated with a fivefold acceleration of gene loss and increased rates of amino acid evolution at receptors that remain intact. Gene loss appears to primarily affect Grs that respond to bitter compounds while elevated Ka/Ks is most pronounced in the subset of Ors that are expressed in larvae. Our results provide strong evidence that the observed phenomena result from the invasion of a novel ecological niche and present a unique synthesis of molecular evolutionary analyses with ecological data.
APPENDIX: Estimating Different Rates of Gene Loss on a Tree
Brian C. O'Meara
Center for Population Biology, University of California, Davis, California 95616
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