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Variation in gene expression within and among natural populations

Nature Genetics volume 32, pages 261–266 (2002)Cite this article

Abstract

Evolution may depend more strongly on variation in gene expression than on differences between variant forms of proteins1. Regions of DNA that affect gene expression are highly variable, containing 0.6% polymorphic sites2. These naturally occurring polymorphic nucleotides can alter in vivo transcription rates3,4,5,6,7. Thus, one might expect substantial variation in gene expression between individuals. But the natural variation in mRNA expression for a large number of genes has not been measured. Here we report microarray studies addressing the variation in gene expression within and between natural populations of teleost fish of the genus Fundulus. We observed statistically significant differences in expression between individuals within the same population for approximately 18% of 907 genes. Expression typically differed by a factor of 1.5, and often more than 2.0. Differences between populations increased the variation. Much of the variation between populations was a positive function of the variation within populations and thus is most parsimoniously described as random. Some genes showed unexpected patterns of expression—changes unrelated to evolutionary distance. These data suggest that substantial natural variation exists in gene expression and that this quantitative variation is important in evolution.

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Figure 1: Loop design used in microarray studies.
Figure 2: Error variance versus significance between individuals within populations.
Figure 3: Frequency distributions of range of gene expression levels among individuals within a population.
Figure 4: Pattern and significance of gene expression between populations.
Figure 5: Variation between and within populations.
Figure 6: Patterns of gene expression for northern F. heteroclitus population versus combined southern F. heteroclitus and F. grandis populations.

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Acknowledgements

This research was supported by a National Science Foundation BioInformatics post-doctoral fellowship to M.F.O., a National Cancer Institute grant to G.A.C. and a National Science Foundation Integrative Biology and Neuroscience grant to D.L.C. Additional support was provided by the School of Biological Science through M. Marino-Carrion. We would like to thank K. Horgan of M.J. Research for arranging the donation of Tetrad-thermal cycler, Motorola for donating the activated slides used in the production of microarrays and AP-Biotech and specifically R. Feldman for use of MegaBace used to re-sequence cDNAs.

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Authors and Affiliations

  1. School of Biological Sciences, 5007 Rockhill Road, University of Missouri-Kansas City, Kansas City, 64110-2499, Missouri, USA

    Marjorie F. Oleksiak & Douglas L. Crawford

  2. The Jackson Laboratory, 600 Main Street, Bar Harbor, 04609, Maine, USA

    Gary A. Churchill

Authors
  1. Marjorie F. Oleksiak
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Correspondence to Douglas L. Crawford.

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Oleksiak, M., Churchill, G. & Crawford, D. Variation in gene expression within and among natural populations. Nat Genet 32, 261–266 (2002). https://doi.org/10.1038/ng983

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