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. 2000 Aug;155(4):1903–1912. doi: 10.1093/genetics/155.4.1903

Molecular evolution of the avian CHD1 genes on the Z and W sex chromosomes.

A K Fridolfsson 1, H Ellegren 1
PMCID: PMC1461215  PMID: 10924484

Abstract

Genes shared between the nonrecombining parts of the two types of sex chromosomes offer a potential means to study the molecular evolution of the same gene exposed to different genomic environments. We have analyzed the molecular evolution of the coding sequence of the first pair of genes found to be shared by the avian Z (present in both sexes) and W (female-specific) sex chromosomes, CHD1Z and CHD1W. We show here that these two genes evolve independently but are highly conserved at nucleotide as well as amino acid levels, thus not indicating a female-specific role of the CHD1W gene. From comparisons of sequence data from three avian lineages, the frequency of nonsynonymous substitutions (K(a)) was found to be higher for CHD1W (1.55 per 100 sites) than for CHD1Z (0.81), while the opposite was found for synonymous substitutions (K(s), 13.5 vs. 22.7). We argue that the lower effective population size and the absence of recombination on the W chromosome will generally imply that nonsynonymous substitutions accumulate faster on this chromosome than on the Z chromosome. The same should be true for the Y chromosome relative to the X chromosome in XY systems. Our data are compatible with a male-biased mutation rate, manifested by the faster rate of neutral evolution (synonymous substitutions) on the Z chromosome than on the female-specific W chromosome.

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Selected References

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  1. Agulnik A. I., Bishop C. E., Lerner J. L., Agulnik S. I., Solovyev V. V. Analysis of mutation rates in the SMCY/SMCX genes shows that mammalian evolution is male driven. Mamm Genome. 1997 Feb;8(2):134–138. doi: 10.1007/s003359900372. [DOI] [PubMed] [Google Scholar]
  2. Alvarez-Valin F., Jabbari K., Bernardi G. Synonymous and nonsynonymous substitutions in mammalian genes: intragenic correlations. J Mol Evol. 1998 Jan;46(1):37–44. doi: 10.1007/pl00006281. [DOI] [PubMed] [Google Scholar]
  3. Carmichael A. N., Fridolfsson A. K., Halverson J., Ellegren H. Male-biased mutation rates revealed from Z and W chromosome-linked ATP synthase alpha-subunit (ATP5A1) sequences in birds. J Mol Evol. 2000 May;50(5):443–447. doi: 10.1007/s002390010046. [DOI] [PubMed] [Google Scholar]
  4. Chang B. H., Li W. H. Estimating the intensity of male-driven evolution in rodents by using X-linked and Y-linked Ube 1 genes and pseudogenes. J Mol Evol. 1995 Jan;40(1):70–77. doi: 10.1007/BF00166597. [DOI] [PubMed] [Google Scholar]
  5. Crow J. F. Molecular evolution--who is in the driver's seat? Nat Genet. 1997 Oct;17(2):129–130. doi: 10.1038/ng1097-129. [DOI] [PubMed] [Google Scholar]
  6. Ellegren H. First gene on the avian W chromosome (CHD) provides a tag for universal sexing of non-ratite birds. Proc Biol Sci. 1996 Dec 22;263(1377):1635–1641. doi: 10.1098/rspb.1996.0239. [DOI] [PubMed] [Google Scholar]
  7. Ellegren H., Fridolfsson A. K. Male-driven evolution of DNA sequences in birds. Nat Genet. 1997 Oct;17(2):182–184. doi: 10.1038/ng1097-182. [DOI] [PubMed] [Google Scholar]
  8. Ellegren H. Evolution of the avian sex chromosomes and their role in sex determination. Trends Ecol Evol. 2000 May;15(5):188–192. doi: 10.1016/s0169-5347(00)01821-8. [DOI] [PubMed] [Google Scholar]
  9. Fridolfsson A. K., Cheng H., Copeland N. G., Jenkins N. A., Liu H. C., Raudsepp T., Woodage T., Chowdhary B., Halverson J., Ellegren H. Evolution of the avian sex chromosomes from an ancestral pair of autosomes. Proc Natl Acad Sci U S A. 1998 Jul 7;95(14):8147–8152. doi: 10.1073/pnas.95.14.8147. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Graves J. A. The evolution of mammalian sex chromosomes and the origin of sex determining genes. Philos Trans R Soc Lond B Biol Sci. 1995 Nov 29;350(1333):305–312. doi: 10.1098/rstb.1995.0166. [DOI] [PubMed] [Google Scholar]
  11. Griffiths R., Daan S., Dijkstra C. Sex identification in birds using two CHD genes. Proc Biol Sci. 1996 Sep 22;263(1374):1251–1256. doi: 10.1098/rspb.1996.0184. [DOI] [PubMed] [Google Scholar]
  12. Griffiths R., Korn R. M. A CHD1 gene is Z chromosome linked in the chicken Gallus domesticus. Gene. 1997 Sep 15;197(1-2):225–229. doi: 10.1016/s0378-1119(97)00266-7. [DOI] [PubMed] [Google Scholar]
  13. Huelsenbeck J. P. Is the Felsenstein zone a fly trap? Syst Biol. 1997 Mar;46(1):69–74. doi: 10.1093/sysbio/46.1.69. [DOI] [PubMed] [Google Scholar]
  14. Hurst L. D., Ellegren H. Sex biases in the mutation rate. Trends Genet. 1998 Nov;14(11):446–452. doi: 10.1016/s0168-9525(98)01577-7. [DOI] [PubMed] [Google Scholar]
  15. Jones R. C., Lin M. Spermatogenesis in birds. Oxf Rev Reprod Biol. 1993;15:233–264. [PubMed] [Google Scholar]
  16. Lahn B. T., Page D. C. Functional coherence of the human Y chromosome. Science. 1997 Oct 24;278(5338):675–680. doi: 10.1126/science.278.5338.675. [DOI] [PubMed] [Google Scholar]
  17. Miyata T., Hayashida H., Kuma K., Mitsuyasu K., Yasunaga T. Male-driven molecular evolution: a model and nucleotide sequence analysis. Cold Spring Harb Symp Quant Biol. 1987;52:863–867. doi: 10.1101/sqb.1987.052.01.094. [DOI] [PubMed] [Google Scholar]
  18. Mouchiroud D., Gautier C., Bernardi G. The compositional distribution of coding sequences and DNA molecules in humans and murids. J Mol Evol. 1988;27(4):311–320. doi: 10.1007/BF02101193. [DOI] [PubMed] [Google Scholar]
  19. Oldenburg J., Schwaab R., Grimm T., Zerres K., Hakenberg P., Brackmann H. H., Olek K. Direct and indirect estimation of the sex ratio of mutation frequencies in hemophilia A. Am J Hum Genet. 1993 Dec;53(6):1229–1238. [PMC free article] [PubMed] [Google Scholar]
  20. Pamilo P., Bianchi N. O. Evolution of the Zfx and Zfy genes: rates and interdependence between the genes. Mol Biol Evol. 1993 Mar;10(2):271–281. doi: 10.1093/oxfordjournals.molbev.a040003. [DOI] [PubMed] [Google Scholar]
  21. Raymond C. S., Kettlewell J. R., Hirsch B., Bardwell V. J., Zarkower D. Expression of Dmrt1 in the genital ridge of mouse and chicken embryos suggests a role in vertebrate sexual development. Dev Biol. 1999 Nov 15;215(2):208–220. doi: 10.1006/dbio.1999.9461. [DOI] [PubMed] [Google Scholar]
  22. Schorderet D. F., Gartler S. M. Analysis of CpG suppression in methylated and nonmethylated species. Proc Natl Acad Sci U S A. 1992 Feb 1;89(3):957–961. doi: 10.1073/pnas.89.3.957. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Shimmin L. C., Chang B. H., Li W. H. Male-driven evolution of DNA sequences. Nature. 1993 Apr 22;362(6422):745–747. doi: 10.1038/362745a0. [DOI] [PubMed] [Google Scholar]
  24. Smith C. A., McClive P. J., Western P. S., Reed K. J., Sinclair A. H. Conservation of a sex-determining gene. Nature. 1999 Dec 9;402(6762):601–602. doi: 10.1038/45130. [DOI] [PubMed] [Google Scholar]
  25. Smith N. G., Hurst L. D. Molecular evolution of an imprinted gene: repeatability of patterns of evolution within the mammalian insulin-like growth factor type II receptor. Genetics. 1998 Oct;150(2):823–833. doi: 10.1093/genetics/150.2.823. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Smith N. G., Hurst L. D. The causes of synonymous rate variation in the rodent genome. Can substitution rates be used to estimate the sex bias in mutation rate? Genetics. 1999 Jun;152(2):661–673. doi: 10.1093/genetics/152.2.661. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Stefos K., Arrighi F. E. Heterochromatic nature of W chromosome in birds. Exp Cell Res. 1971 Sep;68(1):228–231. doi: 10.1016/0014-4827(71)90611-2. [DOI] [PubMed] [Google Scholar]
  28. Stokes D. G., Perry R. P. DNA-binding and chromatin localization properties of CHD1. Mol Cell Biol. 1995 May;15(5):2745–2753. doi: 10.1128/mcb.15.5.2745. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Stokes D. G., Tartof K. D., Perry R. P. CHD1 is concentrated in interbands and puffed regions of Drosophila polytene chromosomes. Proc Natl Acad Sci U S A. 1996 Jul 9;93(14):7137–7142. doi: 10.1073/pnas.93.14.7137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Tricome J. R., Muhammad N., Swieck S. W., Rice J. J. A team approach to the transfer of robotics from technical services to a QC environment. J Automat Chem. 1996;18(4):143–146. doi: 10.1155/S1463924696000132. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Tucker P. K., Lundrigan B. L. Rapid evolution of the sex determining locus in Old World mice and rats. Nature. 1993 Aug 19;364(6439):715–717. doi: 10.1038/364715a0. [DOI] [PubMed] [Google Scholar]
  32. Whitfield L. S., Lovell-Badge R., Goodfellow P. N. Rapid sequence evolution of the mammalian sex-determining gene SRY. Nature. 1993 Aug 19;364(6439):713–715. doi: 10.1038/364713a0. [DOI] [PubMed] [Google Scholar]
  33. Woodage T., Basrai M. A., Baxevanis A. D., Hieter P., Collins F. S. Characterization of the CHD family of proteins. Proc Natl Acad Sci U S A. 1997 Oct 14;94(21):11472–11477. doi: 10.1073/pnas.94.21.11472. [DOI] [PMC free article] [PubMed] [Google Scholar]

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