Adaptive Evolution of Metabolic Pathways in Drosophila

Abstract

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.

Department(s)

Biological Sciences

Comments

This article is corrected by an erratum.

Keywords and Phrases

fructose bisphosphate aldolase; gene product; glucose 6 phosphatase; glucose 6 phosphate; glucose 6 phosphate dehydrogenase; phosphoglucomutase; synthetase; trehalose 6 phosphate synthetase; unclassified drug; adaptive behavior; animal cell; animal tissue; catalysis; DNA polymorphism; Drosophila; Drosophila melanogaster; Drosophila simulans; enzyme analysis; gene locus; genetic analysis; gluconeogenesis; glycolysis; metabolic regulation; molecular evolution; natural selection; neutral gene theory; nonhuman; nucleotide sequence; population genetic parameters; adaptation; animal; genetics; metabolism; molecular genetics; Physiological; Animals; Evolution; Molecular; Metabolic Networks and Pathways; Molecular Sequence Data; Network evolution; Population genomics; Positive selection; Systems biology

International Standard Serial Number (ISSN)

0737-4038

Document Type

Article - Journal

Document Version

Citation

File Type

text

Language(s)

English

Rights

© 2007 Society for Molecular Biology and Evolution, All rights reserved.

Publication Date

01 Mar 2007

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