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Nature 438, 220-223 (10 November 2005) | doi:10.1038/nature04114; Received 26 April 2005; Accepted 2 August 2005

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A mutation accumulation assay reveals a broad capacity for rapid evolution of gene expression

Scott A. Rifkin1,2,5, David Houle3, Junhyong Kim4 & Kevin P. White1,2

  1. Department of Ecology and Evolutionary Biology, Yale University, PO Box 208106, New Haven, Connecticut 06520-8106, USA
  2. Department of Genetics, Yale University School of Medicine, PO Box 208005, New Haven, Connecticut 06520-8005, USA
  3. Department of Biological Science, Florida State University, Tallahassee, Florida 32306-1100, USA
  4. Department of Biology, University of Pennsylvania, 203 Goddard Laboratories, 415 South University Avenue, Philadelphia, Pennsylvania 19104, USA
  5. †Present address: Department of Organismic and Evolutionary Biology, Harvard University, 16 Divinity Avenue, Cambridge, Massachusetts 02138, USA

Correspondence to: Junhyong Kim4Kevin P. White1,2 Correspondence and requests for materials should be addressed to J.K. (Email: junhyong@sas.upenn.edu) or K.P.W. (Email: kevin.white@yale.edu). Microarray data have been deposited in the Gene Expression Omnibus under accession numbers GSE2126 (mutation accumulation lines), GSE2641 (technical error) and GSE2642 (comparative data update and extension).

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Mutation is the ultimate source of biological diversity because it generates the variation that fuels evolution1. Gene expression is the first step by which an organism translates genetic information into developmental change. Here we estimate the rate at which mutation produces new variation in gene expression by measuring transcript abundances across the genome during the onset of metamorphosis in 12 initially identical Drosophila melanogaster lines that independently accumulated mutations for 200 generations2. We find statistically significant mutational variation for 39% of the genome and a wide range of variability across corresponding genes. As genes are upregulated in development their variability decreases, and as they are downregulated it increases, indicating that developmental context affects the evolution of gene expression. A strong correlation between mutational variance and environmental variance shows that there is the potential for widespread canalization3. By comparing the evolutionary rates that we report here with differences between species4, 5, we conclude that gene expression does not evolve according to strictly neutral models. Although spontaneous mutations have the potential to generate abundant variation in gene expression, natural variation is relatively constrained.