The transcriptional consequences of mutation and natural selection in Caenorhabditis elegans

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Abstract

The evolutionary importance of gene-expression divergence is unclear: some studies suggest that it is an important mechanism for evolution by natural selection1,2, whereas others claim that most between-species regulatory changes are neutral or nearly neutral3. We examined global transcriptional divergence patterns in a set of Caenorhabditis elegans mutation-accumulation lines and natural isolate lines to provide insights into the evolutionary importance of transcriptional variation and to discriminate between the forces of mutation and natural selection in shaping the evolution of gene expression. We detected the effects of selection on transcriptional divergence patterns and characterized them with respect to coexpressed gene sets, chromosomal clustering of expression changes and functional gene categories. We directly compared observed transcriptional variation patterns in the mutation-accumulation and natural isolate lines to a neutral model of transcriptome evolution to show that strong stabilizing selection dominates the evolution of transcriptional change for thousands of C. elegans expressed sequences.

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Figure 1: Half-volcano plots for MA and NI microarray data.
Figure 2: Distributions of differentially expressed genes in coexpression mounts.
Figure 3: Physical distances between differentially expressed genes in the MA lines.

References

  1. 1

    King, M.-C. & Wilson, A.C. Evolution at two levels in humans and chimpanzees. Science 188, 107–116 (1975).

  2. 2

    Oleksiak, M.F., Churchill, G.A. & Crawford, D.L. Variation in gene expression within and among natural populations. Nat. Genet. 32, 261–266 (2002).

  3. 3

    Khaitovich, P. et al. A neutral model of transcriptome evolution. PLoS Biol. 2, 682–689 (2004).

  4. 4

    Vassilieva, L.L., Hook, A.M. & Lynch, M. The fitness effects of spontaneous mutations in Caenorhabditis elegans. Evolution 54, 1234–1246 (2000).

  5. 5

    Lynch, M. & Conery, J.S. The origins of genome complexity. Science 302, 1401–1404 (2003).

  6. 6

    Graustein, A., Gaspar, J.M., Walters, J.R. & Palopoli, M.F. Levels of DNA polymorphism vary with mating system in the nematode genus Caenorhabditis. Genetics 161, 99–107 (2002).

  7. 7

    Denver, D.R., Morris, K., Lynch, M. & Thomas, W.K. High mutation rate and predominace of insertions in the Caenorhabditis elegans nuclear genome. Nature 430, 679–682 (2004).

  8. 8

    Charlesworth, B. Effective population size. Curr. Biol. 12, R716–R717 (2002).

  9. 9

    Kerr, M.K. & Churchill, G.A. Experimental design for gene expression microarrays. Biostatistics 2, 183–201 (2001).

  10. 10

    Denver, D.R., Morris, K. & Thomas, W.K. Phylogenetics in Caenorhabditis elegans: an analysis of divergence and outcrossing. Mol. Biol. Evol. 20, 393–400 (2003).

  11. 11

    Cui, X. & Churchill, G.A. Statistical tests for differential expression in cDNA microarray experiments. Genome Biol. 4, 210 (2003).

  12. 12

    Wittkopp, P.J., Haerum, B.K. & Clark, A.G. Evolutionary changes in cis and trans gene regulation. Nature 430, 85–88 (2004).

  13. 13

    Wray, G.A. et al. The evolution of transcriptional regulation in eukaryotes. Mol. Biol. Evol. 20, 1377–1419 (2003).

  14. 14

    Kim, S.K. et al. A gene expression map for Caenorhabditis elegans. Science 293, 2087–2092 (2001).

  15. 15

    Barnes, T.M., Kohara, Y., Coulson, A. & Hekimi, S. Meiotic recombination, noncoding DNA and genomic organization in Caenorhabditis elegans. Genetics 141, 159–179 (1995).

  16. 16

    Koch, R., van Luenen, H.G., van der Horst, M., Thijssen, K.L. & Plasterk, R.H. Single nucleotide polymorphisms in wild isolates of Caenorhabditis elegans. Genome Res. 10, 1690–1696 (2000).

  17. 17

    Hill, W.G. & Robertson, A. The effects of linkage on limits to artificial selection. Genet. Res. 8, 269–294 (1966).

  18. 18

    The C. elegans Sequencing Consortium. Genome sequence of the nematode C. elegans: a platform for investigating biology. Science 282, 2012–2018 (1998).

  19. 19

    Roy, P.J., Stuart, J.M., Lund, J. & Kim, S.K. Chromosomal clustering of muscle-expressed genes in Caenorhabditis elegans. Nature 418, 975–979 (2002).

  20. 20

    Lercher, M.L., Blumenthal, T. & Hurst, L.D. Coexpression of neighboring genes in Caenorhabditis elegans is mostly due to operons and duplicate genes. Genome Res. 13, 238–243 (2003).

  21. 21

    Lynch, M. & Hill, W.G. Phenotypic evolution by neutral mutation. Evolution 40, 915–935 (1986).

  22. 22

    Hsieh, W., Chu, T., Wolfinger, R.D. & Gibson, G. Mixed-model reanalysis of primate data suggests tissue and species biases in oligonucleotide-based gene expression profiles. Genetics 165, 747–757 (2003).

  23. 23

    Enard, W. et al. Intra- and interspecific variation in primate gene expression patterns. Science 296, 340–343 (2002).

  24. 24

    Ashburner, M. et al. Gene ontology: tool for the unification of biology. Gene Ontology Consortium. Nat. Genet. 25, 25–29 (2000).

  25. 25

    Harris, T.W. et al. WormBase: a multi-species resource for nematode biology and genomics. Nucleic Acids Res. 32, D411–D417 (2004).

  26. 26

    Fabian, T.J. & Johnson, T.E. Production of age-synchronous mass cultures of Caenorhabditis elegans. J. Gerontol. 49, B145–B156 (1994).

  27. 27

    Jiang, M. et al. Genome-wide analysis of developmental and sex-regulated gene expression profiles in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 98, 218–223 (2001).

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Acknowledgements

We thank K. Duke and M. Jiang for cDNA syntheses and microarray hybridizations and scanning, H. Wu for help with R/MAANOVA, T.D. Kocher for insightful comments and the Caenorhabditis Genetics Center for providing the C. elegans natural isolates. This work was supported by a University of Missouri Research Board grant (to W.K.T.) and US National Institutes of Health grant (to M.L. and W.K.T.). D.R.D. was supported by a US National Institutes of Health National Research Service Award fellowship, and J.T.S. was supported by a postdoctoral fellowship from the Alfred P. Sloan Foundation.

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Correspondence to Dee R Denver.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Fig. 1

Microarray experimental design. (PDF 113 kb)

Supplementary Fig. 2

MA line-specific expression ratios for mount genes. (PDF 1075 kb)

Supplementary Fig. 3

Observed Vg/Vm ratios for gene expression. (PDF 69 kb)

Supplementary Table 1

Differentially-expressed genes in the MA lines. (PDF 404 kb)

Supplementary Table 2

Differentially-expressed genes in the NI lines. (PDF 97 kb)

Supplementary Note (PDF 52 kb)

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