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Constraint and turnover in sex-biased gene expression in the genus Drosophila

Nature volume 450, pages 233–237 (2007)Cite this article

Abstract

Both genome content and deployment contribute to phenotypic differences between species1,2,3,4,5. Sex is the most important difference between individuals in a species and has long been posited to be rapidly evolving. Indeed, in the Drosophila genus, traits such as sperm length, genitalia, and gonad size are the most obvious differences between species6. Comparative analysis of sex-biased expression should deepen our understanding of the relationship between genome content and deployment during evolution. Using existing7,8 and newly assembled genomes9, we designed species-specific microarrays to examine sex-biased expression of orthologues and species-restricted genes in D. melanogaster, D. simulans, D. yakuba, D. ananassae, D. pseudoobscura, D. virilis and D. mojavensis. We show that averaged sex-biased expression changes accumulate monotonically over time within the genus. However, different genes contribute to expression variance within species groups compared to between groups. We observed greater turnover of species-restricted genes with male-biased expression, indicating that gene formation and extinction may play a significant part in species differences. Genes with male-biased expression also show the greatest expression and DNA sequence divergence. This higher divergence and turnover of genes with male-biased expression may be due to high transcription rates in the male germline, greater functional pleiotropy of genes expressed in females, and/or sexual competition.

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Figure 1: Sex-biased expression in Drosophila species.
Figure 2: Expression divergence among common orthologues.
Figure 3: Expression divergence within and between species and groups.
Figure 4: Relationship between sex-biased expression, gene content and sequence divergence.

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References

  1. Denver, D. R. et al. The transcriptional consequences of mutation and natural selection in Caenorhabditis elegans . Nature Genet. 37, 544–548 (2005)

    Article  CAS  PubMed  Google Scholar 

  2. Jordan, I. K., Marino-Ramirez, L. & Koonin, E. V. Evolutionary significance of gene expression divergence. Gene 345, 119–126 (2005)

    Article  CAS  PubMed  Google Scholar 

  3. Khaitovich, P., Enard, W., Lachmann, M. & Paabo, S. Evolution of primate gene expression. Nature Rev. Genet. 7, 693–702 (2006)

    Article  CAS  PubMed  Google Scholar 

  4. Rifkin, S. A., Houle, D., Kim, J. & White, K. P. A mutation accumulation assay reveals a broad capacity for rapid evolution of gene expression. Nature 438, 220–223 (2005)

    Article  ADS  CAS  PubMed  Google Scholar 

  5. Rifkin, S. A., Kim, J. & White, K. P. Evolution of gene expression in the Drosophila melanogaster subgroup. Nature Genet. 33, 138–144 (2003)

    Article  CAS  PubMed  Google Scholar 

  6. Powell, J. R. Progress and Prospects in Evolutionary Biology: The Drosophila Model (Oxford Univ. Press, Oxford, 1997)

    Google Scholar 

  7. Adams, M. D. et al. The genome sequence of Drosophila melanogaster . Science 287, 2185–2195 (2000)

    Article  PubMed  Google Scholar 

  8. Richards, S. et al. Comparative genome sequencing of Drosophila pseudoobscura: chromosomal, gene, and cis-element evolution. Genome Res. 15, 1–18 (2005)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Drosophila 12 Genomes Consortium. Evolution of genes and genomes in the Drosophila phylogeny. Nature doi: 10.1038/nature06341 (this issue)

  10. Ellegren, H. & Parsch, J. The evolution of sex-biased genes and sex-biased gene expression. Nature Rev. Genet. 8, 689–698 (2007)

    Article  CAS  PubMed  Google Scholar 

  11. Tamura, K., Subramanian, S. & Kumar, S. Temporal patterns of fruit fly (Drosophila) evolution revealed by mutation clocks. Mol. Biol. Evol. 21, 36–44 (2004)

    Article  CAS  PubMed  Google Scholar 

  12. Nuzhdin, S. V., Wayne, M. L., Harmon, K. L. & McIntyre, L. M. Common pattern of evolution of gene expression level and protein sequence in Drosophila . Mol. Biol. Evol. 21, 1308–1317 (2004)

    Article  CAS  PubMed  Google Scholar 

  13. Ranz, J. M., Castillo-Davis, C. I., Meiklejohn, C. D. & Hartl, D. L. Sex-dependent gene expression and evolution of the Drosophila transcriptome. Science 300, 1742–1745 (2003)

    Article  ADS  CAS  PubMed  Google Scholar 

  14. Harris, M. A. et al. The Gene Ontology (GO) database and informatics resource. Nucleic Acids Res. 32, D258–D261 (2004)

    Article  ADS  CAS  PubMed  Google Scholar 

  15. Ohta, T. & Gillespie, J. H. Development of neutral and nearly neutral theories. Theor. Popul. Biol. 49, 128–142 (1996)

    Article  CAS  PubMed  Google Scholar 

  16. Hsieh, W. P., Chu, T. M., 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)

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Khaitovich, P., Paabo, S. & Weiss, G. Toward a neutral evolutionary model of gene expression. Genetics 170, 929–939 (2005)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Lemos, B., Meiklejohn, C. D., Caceres, M. & Hartl, D. L. Rates of divergence in gene expression profiles of primates, mice, and flies: stabilizing selection and variability among functional categories. Evolution Int. J. Org. Evolution 59, 126–137 (2005)

    Article  CAS  Google Scholar 

  19. Wray, G. A. The evolutionary significance of cis-regulatory mutations. Nature Rev. Genet. 8, 206–216 (2007)

    Article  CAS  PubMed  Google Scholar 

  20. Li, W. H. Unbiased estimation of the rates of synonymous and nonsynonymous substitution. J. Mol. Evol. 36, 96–99 (1993)

    Article  CAS  PubMed  Google Scholar 

  21. Khaitovich, P. et al. Parallel patterns of evolution in the genomes and transcriptomes of humans and chimpanzees. Science 309, 1850–1854 (2005)

    Article  ADS  CAS  PubMed  Google Scholar 

  22. Subramanian, S. & Kumar, S. Gene expression intensity shapes evolutionary rates of the proteins encoded by the vertebrate genome. Genetics 168, 373–381 (2004)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Miller, G. T. & Pitnick, S. Sperm-female coevolution in Drosophila . Science 298, 1230–1233 (2002)

    Article  ADS  CAS  PubMed  Google Scholar 

  24. FitzGerald, P. C., Sturgill, D., Shyakhtenko, A., Oliver, B. & Vinson, C. Comparative genomics of Drosophila and human core promoters. Genome Biol. 7, R53 (2006)

    Article  PubMed  PubMed Central  Google Scholar 

  25. Schmidt, E. E. & Schibler, U. High accumulation of components of the RNA polymerase II transcription machinery in rodent spermatids. Development 121, 2373–2383 (1995)

    CAS  PubMed  Google Scholar 

  26. Struhl, K. Transcriptional noise and the fidelity of initiation by RNA polymerase II. Nature Struct. Mol. Biol. 14, 103–105 (2007)

    Article  CAS  Google Scholar 

  27. Perrimon, N., Mohler, D., Engstrom, L. & Mahowald, A. P. X-linked female-sterile loci in Drosophila melanogaster . Genetics 113, 695–712 (1986)

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Parisi, M. et al. A survey of ovary-, testis-, and soma-biased gene expression in Drosophila melanogaster adults. Genome Biol. 5, R40 (2004)

    Article  PubMed  PubMed Central  Google Scholar 

  29. Singh, S. R., Singh, B. N. & Hoenigsberg, H. F. Female remating, sperm competition and sexual selection in Drosophila . Genet. Mol. Res. 1, 178–215 (2002)

    PubMed  Google Scholar 

  30. Parra, G., Blanco, E. & Guigo, R. GeneID in Drosophila . Genome Res. 10, 511–515 (2000)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Grumbling, G. & Strelets, V. FlyBase: anatomical data, images and queries. Nucleic Acids Res. 34, D484–D488 (2006)

    Article  CAS  PubMed  Google Scholar 

  32. Benson, D. A., Karsch-Mizrachi, I., Lipman, D. J., Ostell, J. & Wheeler, D. L. GenBank. Nucleic Acids Res. 34, D16–D20 (2006)

    Article  CAS  PubMed  Google Scholar 

  33. Kent, W. J. BLAT–the BLAST-like alignment tool. Genome Res. 12, 656–664 (2002)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Huber, W., von Heydebreck, A., Sultmann, H., Poustka, A. & Vingron, M. Variance stabilization applied to microarray data calibration and to the quantification of differential expression. Bioinformatics 18 (Suppl 1). S96–S104 (2002)

    Article  PubMed  Google Scholar 

  35. Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. Roy. Statist. Soc. Ser. B. Methodological 57, 289–300 (1995)

    MathSciNet  MATH  Google Scholar 

  36. Charif, D. & Lobry, J. R. in Structural approaches to sequence evolution: Molecules, networks, populations (eds Bastolla, U. M.P., Roman, H. E. and Vendruscolo, M.). (2006)

    Google Scholar 

  37. Tamura, K., Dudley, J., Nei, M. & Kumar, S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) Software Version 4.0. Mol. Biol. Evol. 24, 1596–1599 (2007)

    Article  CAS  PubMed  Google Scholar 

  38. de Hoon, M. J., Imoto, S., Nolan, J. & Miyano, S. Open source clustering software. Bioinformatics 20, 1453–1454 (2004)

    Article  CAS  PubMed  Google Scholar 

  39. Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215, 403–410 (1990)

    Article  CAS  PubMed  Google Scholar 

  40. Gentleman, R. C. et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5, R80 (2004)

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank the Drosophila Comparative Genome Sequencing and Analysis Consortium for access to the assembly, alignment and annotation of the 12 sequenced Drosophila genomes, S. Davis for valuable technical advice, and K. P. White, C. Vinson, A. Clark, M. Lynch and members of the Oliver laboratory for helpful discussion and comments on the manuscript. We are supported by the Intramural Research Program of the NIH, NIDDK, except S.K. who is supported by the NIH Extramural Program.

Author information

Author notes

  1. Michael Parisi

    Present address: Present address: Department of Biology, University of Pennsylvania, Pennsylvania 19104, USA.,

  2. Yu Zhang and David Sturgill: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Health and Human Services, Laboratory of Cellular and Developmental Biology, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, Maryland 20892, USA,

    Yu Zhang, David Sturgill, Michael Parisi & Brian Oliver

  2. Center for Evolutionary Functional Genomics, Biodesign Institute, Arizona State University, Tempe, Arizona 85287, USA ,

    Sudhir Kumar

Authors
  1. Yu Zhang
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  2. David Sturgill
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Corresponding authors

Correspondence to Yu Zhang or Brian Oliver.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

The file contains supplementary Figures S1-S5 with Legends and Supplementary Tables S1-S2. (PDF 1056 kb)

Supplementary Table

The file contains Supplementary Table S3-S16 for the list of genes with female-biased and male-biased expression in all seven species separately. (XLS 3513 kb)

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Zhang, Y., Sturgill, D., Parisi, M. et al. Constraint and turnover in sex-biased gene expression in the genus Drosophila. Nature 450, 233–237 (2007). https://doi.org/10.1038/nature06323

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