Abstract
In Drosophila, there is a consistent deficit of male-biased genes on the X chromosome. It has been suggested that male-biased genes may evolve from initially unbiased genes as a result of increased expression levels in males. If transcription rates are limited, a large increase in expression in the testis may be harder to achieve for single-copy X-linked genes than for autosomal genes, because they are already hypertranscribed due to dosage compensation. This hypothesis predicts that the larger the increase in expression required to make a male-biased gene, the lower the chance of this being achievable if it is located on the X chromosome. Consequently, highly expressed male-biased genes should be located on the X chromosome less often than lowly expressed male-biased genes. This pattern is observed in our analysis of publicly available data, where microarray data or EST data are used to detect male-biased genes in D. melanogaster and to measure their expression levels. This is consistent with the idea that limitations in transcription rates may prevent male-biased genes from accumulating on the X chromosome.
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References
Betrán E, Thornton K, Long M (2002) Retroposed new genes out of the X in Drosophila. Genome Res 12:1854–1859
Charlesworth B (1978) Model for evolution of Y chromosomes and dosage compensation. Proc Natl Acad Sci USA 75:5618–5622
Charlesworth B, Coyne JA, Barton NH (1987) The relative rates of evolution of sex-chromosomes and autosomes. Am Nat 130:113–146
Connallon T, Knowles LL (2005) Intergenomic conflict revealed by patterns of sex-biased gene expression. Trends Genet 21:495–499
Drummond DA, Wilke CO (2008) Mistranslation-induced protein misfolding as a dominant constraint on coding-sequence evolution. Cell 134:341–352
Ellegren H, Parsch J (2007) The evolution of sex-biased genes and sex-biased gene expression. Nat Rev Genet 8:689–698
Emerson JJ, Cardoso-Moreira M, Borevitz JO, Long M (2008) Natural selection shapes genome-wide patterns of copy-number polymorphism in Drosophila melanogaster. Science 320:1629–1631
Gupta V, Parisi M, Sturgill D, Nuttall R, Doctolero M, Dudko OK, Malley JD, Eastman PS, Oliver B (2006) Global analysis of X-chromosome dosage compensation. J Biol 5:3.1–3.10
Hense W, Baines JF, Parsch J (2007) X chromosome inactivation during Drosophila spermatogenesis. PLoS Biol 5:e273
Kaiser VB, Ellegren H (2006) Nonrandom distribution of genes with sex-biased expression in the chicken genome. Evol Int J Org Evol 60:1945–1951
Khil PP, Smirnova NA, Romanienko PJ, Camerini-Otero RD (2004) The mouse X chromosome is enriched for sex-biased genes not subject to selection by meiotic sex chromosome inactivation. Nat Genet 36:642–646
Kondrashov FA, Rogozin IB, Wolf YI, Koonin EV (2002) Selection in the evolution of gene duplications. Genome Biol 3:RESEARCH0008
Lercher MJ, Urrutia AO, Hurst LD (2003) Evidence that the human X chromosome is enriched for male-specific but not female-specific genes. Mol Biol Evol 20:1113–1116
Lin H, Gupta V, Vermilyea MD, Falciani F, Lee JT, O’Neill LP, Turner BM (2007) Dosage compensation in the mouse balances up-regulation and silencing of X-linked genes. PLoS Biol 5:e326
Nguyen DK, Disteche CM (2006) Dosage compensation of the active X chromosome in mammals. Nat Genet 38:47–53
Ohno S (1967) Sex chromosomes and sex-linked genes. Springer, New York
Parisi M, Nuttall R, Naiman D, Bouffard G, Malley J, Andrews J, Eastman S, Oliver B (2003) Paucity of genes on the Drosophila X chromosome showing male-biased expression. Science 299:697–700
Reinke V, Gil IS, Ward S, Kazmer K (2004) Genome-wide germline-enriched and sex-biased expression profiles in Caenorhabditis elegans. Development 131:311–323
Rice WR (1984) Sex chromosomes and the evolution of sexual dimorphism. Evolution 38:735–742
Schwab M (1999) Oncogene amplification in solid tumors. Semin Cancer Biol 9:319–325
Seoighe C, Wolfe KH (1999) Yeast genome evolution in the post-genome era. Curr Opin Microbiol 2:548–554
Straub T, Becker PB (2007) Dosage compensation: the beginning and end of generalization. Nat Rev Genet 8:47–57
Sturgill D, Zhang Y, Parisi M, Oliver B (2007) Demasculinization of X chromosomes in the Drosophila genus. Nature 450:238–241
Vicoso B, Charlesworth B (2006) Evolution on the X chromosome: unusual patterns and processes. Nat Rev Genet 7:645–653
Wang PJ, McCarrey JR, Yang F, Page DC (2001) An abundance of X-linked genes expressed in spermatogonia. Nat Genet 27:422–426
Wu C-I, Xu EY (2003) Sexual antagonism and X inactivation—the SAXI hypothesis. Trends Genet 19:243–247
Zhang Y, Sturgill D, Parisi M, Kumar S, Oliver B (2007) Constraint and turnover in sex-biased gene expression in the genus Drosophila. Nature 450:233–237
Acknowledgments
We thank two referees for very helpful comments on the manuscript. This work was funded by a Portuguese Foundation for Science and Technology scholarship to B.V., and B.C. was supported by the Royal Society.
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Vicoso, B., Charlesworth, B. The Deficit of Male-Biased Genes on the D. melanogaster X Chromosome Is Expression-Dependent: A Consequence of Dosage Compensation?. J Mol Evol 68, 576–583 (2009). https://doi.org/10.1007/s00239-009-9235-4
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DOI: https://doi.org/10.1007/s00239-009-9235-4