Variation in gene expression within and among natural populations

Oleksiak, Marjorie F.; Churchill, Gary A.; Crawford, Douglas L.

doi:10.1038/ng983

Cited by 745Genetic diversity and population structureEvolution and Genetic DynamicsChromosomal and Genetic Variations

Variation in gene expression within and among natural populations

Oleksiak, Marjorie F., Churchill, Gary A., Crawford, Douglas L.·2002·Nature Genetics

DOI 10.1038/ng983

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Abstract

Evolution may depend more strongly on variation in gene expression than on differences between variant forms of proteins. Regions of DNA that affect gene expression are highly variable, containing 0.6% polymorphic sites. These naturally occurring polymorphic nucleotides can alter in vivo transcription rates. 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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Molecular Evolutionary Genetics
Nei, M. (1987) · Columbia University Press eBooks · doi:10.7312/nei-92038 · Cited by 16,583 · see citing works
Cluster analysis and display of genome-wide expression patterns
Eisen, M. B., Spellman, P. T., Brown, P. O., & Botstein, D. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.25.14863 · Cited by 12,617 · see citing works
Molecular classification of cancer: class discovery and class prediction by gene expression monitoring
Golub, T. R., Slonim, D. K., Tamayo, P., Huard, C., Gaasenbeek, M., Mesirov, J. P., Coller, H., Loh, M. L., Downing, J. R., Caligiuri, M. A., et al. (1999) · Science · doi:10.1126/science.286.5439.531 · Cited by 11,516 · see citing works
Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling
Alizadeh, A. A., Eisen, M. B., Davis, R. E., Ma, C., Lossos, I. S., Rosenwald, A., Boldrick, J. C., Sabet, H., Tran, T., Yu, X., et al. (2000) · Nature · doi:10.1038/35000501 · Cited by 9,925 · see citing works
Evolution at Two Levels in Humans and Chimpanzees: Their macromolecules are so alike that regulatory mutations may account for their biological differences
King, M.-C., & Wilson, A. C. (1975) · Science · doi:10.1126/science.1090005 · Cited by 2,815 · see citing works
Resampling-Based Multiple Testing: Examples and Methods for p-Value Adjustment
Martín, M. A., Westfall, P. H., & Young, S. (1993) · Biometrics · doi:10.2307/2533464 · Cited by 2,308 · see citing works
Use of a cDNA microarray to analyse gene expression patterns in human cancer
DeRisi, J. L., Penland, L., Brown, P. O., Bittner, M. L., Meltzer, P. S., Ray, M., Chen, Y.-W., Su, Y. A., & Trent, J. M. (1996) · Nature Genetics · doi:10.1038/ng1296-457 · Cited by 1,952 · see citing works
Genetic Dissection of Transcriptional Regulation in Budding Yeast
Brem, R. B., Yvert, G., Clinton, R., & Kruglyak, L. (2002) · Science · doi:10.1126/science.1069516 · Cited by 1,392 · see citing works
Analysis of Variance for Gene Expression Microarray Data
Kerr, K. F., Martin, M., & Churchill, G. A. (2000) · Journal of Computational Biology · doi:10.1089/10665270050514954 · Cited by 1,310 · see citing works
Haplotype Variation and Linkage Disequilibrium in 313 Human Genes
Stephens, J. C., Schneider, J. A., Tanguay, D. A., Choi, J. Y., Acharya, T., Stanley, S. E., Jiang, R., Messer, C. J., Chew, A., Han, J.-H., et al. (2001) · Science · doi:10.1126/science.1059431 · Cited by 873 · see citing works
Intra- and Interspecific Variation in Primate Gene Expression Patterns
Enard, W., Khaitovich, P., Klose, J., Zöllner, S. K., Heißig, F., Giavalisco, P., Nieselt, K., Muchmore, E. A., Varki, A. P., Ravid, R., et al. (2002) · Science · doi:10.1126/science.1068996 · Cited by 845 · see citing works
The contributions of sex, genotype and age to transcriptional variance in Drosophila melanogaster
Jin, W., Riley-Berger, R., Wolfinger, R. D., White, K. P., Passador-Gurgel, G., & Gibson, G. C. (2001) · Nature Genetics · doi:10.1038/ng766 · Cited by 644 · see citing works
Statistical design and the analysis of gene expression microarray data
Kerr, K. F., & Churchill, G. A. (2007) · Genetics Research · doi:10.1017/s0016672308009713 · Cited by 561 · see citing works
Statistical design and the analysis of gene expression microarray data
Kerr, K. F., & Churchill, G. A. (2001) · Genetics Research · doi:10.1017/s0016672301005055 · Cited by 501 · see citing works
Summer Home Range and Movements of Fundulus Heteroclitus (Pisces: Cyprinodontidae) in a Tidal Creek
Lotrich, V. A. (1975) · Ecology · doi:10.2307/1935311 · Cited by 236 · see citing works
beta-Thalassemia in American Blacks: novel mutations in the "TATA" box and an acceptor splice site.
Antonarakis, S. E., Irkin, S. H., Cheng, T. C., Scott, A. F., Sexton, J. P., Trusko, S. P., Charache, S., & Kazazian, H. H. (1984) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.81.4.1154 · Cited by 191 · see citing works
Molecular basis of evolutionary adaptation at the lactate dehydrogenase-B locus in the fish Fundulus heteroclitus.
Crawford, D. L., & Powers, D. A. (1989) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.86.23.9365 · Cited by 158 · see citing works
Phylogenetic Analysis of Glycolytic Enzyme Expression
Pierce, V. A., & Crawford, D. L. (1997) · Science · doi:10.1126/science.276.5310.256 · Cited by 104 · see citing works
A single-base substitution in the proximal Sp1 site of the human low density lipoprotein receptor promoter as a cause of heterozygous familial hypercholesterolemia.
Koivisto, U., Palvimo, J. J., Jänne, O. A., & Kontula, K. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.22.10526 · Cited by 102 · see citing works
Differential Gene Expression of Hepatocellular Carcinoma Using cDNA Microarray Analysis
Wy, L., Lai, P. B. S., Leung, M. F., Leung, B. C. S., Wong, N., Chen, G., Leung, T. W. H., & Liew, C. C. (2001) · Oncology Research Featuring Preclinical and Clinical Cancer Therapeutics · doi:10.3727/096504001108747530 · Cited by 80 · see citing works
Evolutionary analysis of TATA-less proximal promoter function
Crawford, D. L., Segal, J. A., & Barnett, J. L. (1999) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a026102 · Cited by 67 · see citing works
Application of DNA Microarrays to Study Human Alcoholism
Lewohl, J. M., Dodd, P. R., Mayfield, R. D., & Harris, R. A. (2001) · Journal of Biomedical Science · doi:10.1007/bf02255968 · Cited by 66 · see citing works
GENE FLOW AND MITOCHONDRIAL DNA VARIATION IN THE KILLIFISH,FUNDULUS HETEROCLITUS
Brown, B. L., & Chapman, R. W. (1991) · Evolution · doi:10.1111/j.1558-5646.1991.tb04381.x · Cited by 58 · see citing works
Functional Effects of a Natural Polymorphism in the Transcriptional Regulatory Sequence of HLA-DQB1
Beaty, J. S., West, K. A., & Nepom, G. T. (1995) · Molecular and Cellular Biology · doi:10.1128/mcb.15.9.4771 · Cited by 55 · see citing works
Utility of Natural Populations for Microarray Analyses: Isolation of Genes Necessary for Functional Genomic Studies
Oleksiak, M. F., Kolell, K. J., & Crawford, D. L. (2001) · Marine Biotechnology · doi:10.1007/s10126-001-0043-0 · Cited by 47 · see citing works
A Study of the Evolutionary Relationships ofFundulusTopminnows (Teleostei: Fundulidae)
WILEY, E. O. (1986) · American Zoologist · doi:10.1093/icb/26.1.121 · Cited by 44 · see citing works
Functional Analyses of Natural Variation in Sp1 Binding Sites of a TATA-Less Promoter
Segal, J. A., Barnett, J. L., & Crawford, D. L. (1999) · Journal of Molecular Evolution · doi:10.1007/pl00006596 · Cited by 40 · see citing works
Intraspecific variation in aerobic metabolism and glycolytic enzyme expression in heart ventricles
Podrabsky, J. E., Javillonar, C., Hand, S. C., & Crawford, D. L. (2000) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.2000.279.6.r2344 · Cited by 33 · see citing works
Phylogenetic Relationships among Nine Species from the Genus Fundulus (Cyprinodontiformes, Fundulidae) Inferred from Sequences of the Cytochrome b Gene
Bernardi, G., & Powers, D. A. (1995) · Copeia · doi:10.2307/1446912 · Cited by 33 · see citing works

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Regulatory polymorphisms underlying complex disease traits.
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Yang, L., Kemadjou, J. R., Zinsmeister, C., Bauer, M. F., Legradi, J., Müller, F., Pankratz, M. J., Jäkel, J., & Strähle, U. (2007) · Genome biology · doi:10.1186/gb-2007-8-10-r227 · Cited by 190 · see citing works
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Singh, A. K., McIntyre, L. M., & Sherman, L. A. (2003) · PLANT PHYSIOLOGY · doi:10.1104/pp.103.024018 · Cited by 179 · see citing works
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Fay, J. C., & Wittkopp, P. J. (2007) · Heredity · doi:10.1038/sj.hdy.6801000 · Cited by 179 · see citing works
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Villanueva, J., Martorella, A. J., Lawlor, K., Philip, J., Fleisher, M., Robbins, R. J., & Tempst, P. (2006) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m600229-mcp200 · Cited by 175 · see citing works
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Thompson, D. A., Regev, A., & Roy, S. (2015) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-100913-012908 · Cited by 170 · see citing works
Determinants of intra-specific variation in basal metabolic rate
Konarzewski, M., & Książek, A. (2012) · Journal of Comparative Physiology B · doi:10.1007/s00360-012-0698-z · Cited by 176 · see citing works
Constitutively High Expression of the Histidine Biosynthetic Pathway Contributes to Nickel Tolerance in Hyperaccumulator Plants
Ingle, R. A., Mugford, S. T., Rees, J. D., Campbell, M. M., & Smith, J. A. C. (2005) · The Plant Cell · doi:10.1105/tpc.104.030577 · Cited by 176 · see citing works
HSP70 heat shock proteins and environmental stress in Antarctic marine organisms: A mini-review.
Clark, M., & Peck, L. (2009) · Marine Genomics · doi:10.1016/j.margen.2009.03.003 · Cited by 168 · see citing works
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van Aggelen, G. C., Ankley, G. T., Baldwin, W. S., Bearden, D. W., Benson, W. H., Chipman, J. K., Collette, T. W., Craft, J. A., Denslow, N. D., Embry, M. R., et al. (2009) · Environmental Health Perspectives · doi:10.1289/ehp.0900985 · Cited by 170 · see citing works
The role of gene expression in ecological speciation
Pavey, S. A., Collin, H., Nosil, P., & Rogers, S. M. (2010) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2010.05765.x · Cited by 166 · see citing works
Low Rates of Expression Profile Divergence in Highly Expressed Genes and Tissue-Specific Genes During Mammalian Evolution
Liao, B., & Zhang, J. (2006) · Molecular Biology and Evolution · doi:10.1093/molbev/msj119 · Cited by 160 · see citing works
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Whitehead, A., Clark, B. W., Reid, N. M., Hahn, M. E., & Nacci, D. E. (2017) · Evolutionary Applications · doi:10.1111/eva.12470 · Cited by 161 · see citing works
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Parallelism in gene transcription among sympatric lake whitefish (Coregonus clupeaformisMitchill) ecotypes
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Hodgins-Davis, A., & Townsend, J. P. (2009) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2009.06.011 · Cited by 147 · see citing works
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Perry, G. H., Melsted, P., Marioni, J. C., Wang, Y., Bainer, R. O., Pickrell, J. K., Michelini, K., Zehr, S. M., Yoder, A. D., Stephens, M., et al. (2011) · Genome Research · doi:10.1101/gr.130468.111 · Cited by 147 · see citing works
Nematode-Induced Changes of Transporter Gene Expression in Arabidopsis Roots
Hammes, U. Z., Schachtman, D. P., Berg, R. H., Nielsen, E., Koch, W., McIntyre, L. M., & Taylor, C. G. (2005) · Molecular Plant-Microbe Interactions · doi:10.1094/mpmi-18-1247 · Cited by 145 · see citing works
Comparative transcriptomics implicates mechanisms of evolved pollution tolerance in a killifish population
Whitehead, A., Triant, D. A., Champlin, D. M., & Nacci, D. E. (2010) · Molecular Ecology · doi:10.1111/j.1365-294x.2010.04829.x · Cited by 140 · see citing works
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Bonneaud, C., Balenger, S. L., Russell, A. F., Zhang, J., Hill, G. E., & Edwards, S. V. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1018580108 · Cited by 139 · see citing works
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Polato, N. R., Voolstra, C. R., Schnetzer, J., DeSalvo, M. K., Randall, C. J., Szmant, A. M., Medina, M., & Baums, I. B. (2010) · PLoS ONE · doi:10.1371/journal.pone.0011221 · Cited by 138 · see citing works
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Hsieh, W., Chu, T., Wolfinger, R. D., & Gibson, G. C. (2003) · Genetics · doi:10.1093/genetics/165.2.747 · Cited by 135 · see citing works
Molecular ecological approaches to studying the evolutionary impact of selective harvesting in wildlife
Coltman, D. W. (2007) · Molecular Ecology · doi:10.1111/j.1365-294x.2007.03414.x · Cited by 135 · see citing works
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Seebacher, F., Brand, M. D., Else, P. L., Guderley, H., Hulbert, A. J., & Moyes, C. D. (2010) · Physiological and Biochemical Zoology · doi:10.1086/649964 · Cited by 133 · see citing works
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Vuylsteke, M., van Eeuwijk, F. A., Hummelen, P. V., Kuiper, M. T. R., & Zabeau, M. (2005) · Genetics · doi:10.1534/genetics.105.041509 · Cited by 131 · see citing works
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Schmid‐Hempel, P. (2021) · doi:10.1093/oso/9780198832140.001.0001 · Cited by 130 · see citing works
Functional genomics of cactus host shifts in Drosophila mojavensis
Matzkin, L. M., Watts, T. D., Bitler, B. G., Machado, C. A., & Markow, T. A. (2006) · Molecular Ecology · doi:10.1111/j.1365-294x.2006.03102.x · Cited by 130 · see citing works
Characterizing natural variation using next-generation sequencing technologies
Gilad, Y., Pritchard, J. K., & Thornton, K. (2009) · Trends in Genetics · doi:10.1016/j.tig.2009.09.003 · Cited by 126 · see citing works

Authors: Oleksiak, M. F., Churchill, G. A., & Crawford, D. L.
Affiliations: University of Missouri–Kansas City (US)
Jackson Laboratory (US)
Corresponding author: Crawford, Douglas L.
ORCID: Oleksiak, Marjorie F.
Churchill, Gary A.
Crawford, Douglas L.
Venue: Nature Genetics
Publisher: Springer Science and Business Media LLC
Published: 2002-09-03
Volume: 32
Issue: 2
Pages: 261-266
ISSN: 1061-4036 (ISSN-L)
1546-1718
DOI: 10.1038/ng983
OpenAlex: W2111696544
Cited by: 736
References: 29
Citations by year: 2026: 4 · 2025: 7 · 2024: 15 · 2023: 8 · 2022: 7 · 2021: 59 · 2020: 20 · 2019: 12 · 2018: 17 · 2017: 24 · 2016: 13 · 2015: 25 · 2014: 31 · 2013: 29 · 2012: 29
FWCI: 26.28
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
Locations: Nature Genetics (publishedVersion)
PubMed (publishedVersion)
The Mouseion at the JAXlibrary (Jackson Laboratory) (submittedVersion)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic diversity and population structure
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
Life Sciences › Agricultural and Biological Sciences › Plant Science › Chromosomal and Genetic Variations
Keywords: gene expression variation, natural genetic variation, Fundulus, teleosts, genetic differentiation, mRNA expression, quantitative genetic variation, gene expression evolution
MeSH terms: Analysis of Variance, Phylogeny, RNA, Messenger, Genetic Variation, Gene Expression, Fundulidae

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Variation in gene expression within and among natural populations

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