MBE Advance Access originally published online on March 22, 2007
Molecular Biology and Evolution 2007 24(6):1347-1354; doi:10.1093/molbev/msm057
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Research Articles |
Adaptive Evolution of Metabolic Pathways in Drosophila
Department of Ecology and Evolution, Stony Brook University
E-mail: jmflower{at}life.bio.sunysb.edu.
Accepted for publication March 15, 2007.
The adaptive significance of enzyme variation has been of central interest in population genetics. Yet, how natural selection operates on enzymes in the larger context of biochemical pathways has not been broadly explored. A basic expectation is that natural selection on metabolic phenotypes will target enzymes that control metabolic flux, but how adaptive variation is distributed among enzymes in metabolic networks is poorly understood. Here, we use population genetic methods to identify enzymes responding to adaptive selection in the pathways of central metabolism in Drosophila melanogaster and Drosophila simulans. We report polymorphism and divergence data for 17 genes that encode enzymes of 5 metabolic pathways that converge at glucose-6-phosphate (G6P). Deviations from neutral expectations were observed at five loci. Of the 10 genes that encode the enzymes of glycolysis, only aldolase (Ald) deviated from neutrality. The other 4 genes that were inconsistent with neutral evolution (glucose-6-phosphate dehydrogenase [G6pd]), phosphoglucomutase [Pgm], trehalose-6-phosphate synthetase [Tps1], and glucose-6phosphatase [G6pase] encode G6P branch point enzymes that catalyze reactions at the entry point to the pentose-phosphate, glycogenic, trehalose synthesis, and gluconeogenic pathways. We reconcile these results with population genetics theory and existing arguments on metabolic regulation and propose that the incidence of adaptive selection in this system is related to the distribution of flux control. The data suggest that adaptive evolution of G6P branch point enzymes may have special significance in metabolic adaptation.
Key Words: positive selection • network evolution • population genomics • adaptation • systems biology
1 Present address: Laboratory of Genomic Diversity, National Cancer Institute, Frederick, Maryland
2 Present address: Department of Biological Sciences, Southern Illinois University, Edwardsville, Illinois
3 Present address: Department of Ecology and Evolutionary Biology, University of Arizona
4 Present address: Department of Biology, University of Pennsylvania