Skip to main content
Genetics logoLink to Genetics
. 2004 May;167(1):367–376. doi: 10.1534/genetics.167.1.367

Evolutionary strata on the chicken Z chromosome: implications for sex chromosome evolution.

Lori-Jayne Lawson Handley 1, Helene Ceplitis 1, Hans Ellegren 1
PMCID: PMC1470863  PMID: 15166161

Abstract

The human X chromosome exhibits four "evolutionary strata," interpreted to represent distinct steps in the process whereby recombination became arrested between the proto X and proto Y. To test if this is a general feature of sex chromosome evolution, we studied the Z-W sex chromosomes of birds, which have female rather than male heterogamety and evolved from a different autosome pair than the mammalian X and Y. Here we analyze all five known gametologous Z-W gene pairs to investigate the "strata" hypothesis in birds. Comparisons of the rates of synonymous substitution and intronic divergence between Z and W gametologs reveal the presence of at least two evolutionary strata spread over the p and q arms of the chicken Z chromosome. A phylogenetic analysis of intronic sequence data from different avian lineages indicates that Z-W recombination ceased in the oldest stratum (on Zq; CHD1Z, HINTZ, and SPINZ) 102-170 million years ago (MYA), before the split of the Neoaves and Eoaves. However, recombination continued in the second stratum (on Zp; UBAP2Z and ATP5A1Z) until after the divergence of extant avian orders, with Z and W diverging 58-85 MYA. Our data suggest that progressive and stepwise cessation of recombination is a general feature behind sex chromosome evolution.

Full Text

The Full Text of this article is available as a PDF (119.5 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Atanassov I., Delichère C., Filatov D. A., Charlesworth D., Negrutiu I., Monéger F. Analysis and evolution of two functional Y-linked loci in a plant sex chromosome system. Mol Biol Evol. 2001 Dec;18(12):2162–2168. doi: 10.1093/oxfordjournals.molbev.a003762. [DOI] [PubMed] [Google Scholar]
  2. Bengtsson B. O., Goodfellow P. N. The effect of recombination between the X and Y chromosomes of mammals. Ann Hum Genet. 1987 Jan;51(Pt 1):57–64. doi: 10.1111/j.1469-1809.1987.tb00865.x. [DOI] [PubMed] [Google Scholar]
  3. Benton M. J. Phylogeny of the major tetrapod groups: morphological data and divergence dates. J Mol Evol. 1990 May;30(5):409–424. doi: 10.1007/BF02101113. [DOI] [PubMed] [Google Scholar]
  4. Ceplitis Helene, Ellegren Hans. Adaptive molecular evolution of HINTW, a female-specific gene in birds. Mol Biol Evol. 2003 Aug 29;21(2):249–254. doi: 10.1093/molbev/msg239. [DOI] [PubMed] [Google Scholar]
  5. Charlesworth B., Charlesworth D. The degeneration of Y chromosomes. Philos Trans R Soc Lond B Biol Sci. 2000 Nov 29;355(1403):1563–1572. doi: 10.1098/rstb.2000.0717. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Charlesworth Deborah. Plant sex determination and sex chromosomes. Heredity (Edinb) 2002 Feb;88(2):94–101. doi: 10.1038/sj.hdy.6800016. [DOI] [PubMed] [Google Scholar]
  7. Cooper A., Penny D. Mass survival of birds across the Cretaceous-Tertiary boundary: molecular evidence. Science. 1997 Feb 21;275(5303):1109–1113. doi: 10.1126/science.275.5303.1109. [DOI] [PubMed] [Google Scholar]
  8. Ellegren H., Carmichael A. Multiple and independent cessation of recombination between avian sex chromosomes. Genetics. 2001 May;158(1):325–331. doi: 10.1093/genetics/158.1.325. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. 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]
  10. Ellegren H. Hens, cocks and avian sex determination. A quest for genes on Z or W? EMBO Rep. 2001 Mar;2(3):192–196. doi: 10.1093/embo-reports/kve050. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. 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]
  12. Ellegren Hans. Dosage compensation: do birds do it as well? Trends Genet. 2002 Jan;18(1):25–28. doi: 10.1016/s0168-9525(01)02553-7. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. Fridolfsson A. K., Ellegren H. Molecular evolution of the avian CHD1 genes on the Z and W sex chromosomes. Genetics. 2000 Aug;155(4):1903–1912. doi: 10.1093/genetics/155.4.1903. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. García-Moreno J., Mindell D. P. Rooting a phylogeny with homologous genes on opposite sex chromosomes (gametologs): a case study using avian CHD. Mol Biol Evol. 2000 Dec;17(12):1826–1832. doi: 10.1093/oxfordjournals.molbev.a026283. [DOI] [PubMed] [Google Scholar]
  16. Graves J. A. Mammals that break the rules: genetics of marsupials and monotremes. Annu Rev Genet. 1996;30:233–260. doi: 10.1146/annurev.genet.30.1.233. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. Hasegawa M., Iida Y., Yano T., Takaiwa F., Iwabuchi M. Phylogenetic relationships among eukaryotic kingdoms inferred from ribosomal RNA sequences. J Mol Evol. 1985;22(1):32–38. doi: 10.1007/BF02105802. [DOI] [PubMed] [Google Scholar]
  19. Hedges S. B., Parker P. H., Sibley C. G., Kumar S. Continental breakup and the ordinal diversification of birds and mammals. Nature. 1996 May 16;381(6579):226–229. doi: 10.1038/381226a0. [DOI] [PubMed] [Google Scholar]
  20. Hori T., Asakawa S., Itoh Y., Shimizu N., Mizuno S. Wpkci, encoding an altered form of PKCI, is conserved widely on the avian W chromosome and expressed in early female embryos: implication of its role in female sex determination. Mol Biol Cell. 2000 Oct;11(10):3645–3660. doi: 10.1091/mbc.11.10.3645. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Härlid A., Janke A., Arnason U. The complete mitochondrial genome of Rhea americana and early avian divergences. J Mol Evol. 1998 Jun;46(6):669–679. doi: 10.1007/pl00006347. [DOI] [PubMed] [Google Scholar]
  22. Itoh Y., Hori T., Saitoh H., Mizuno S. Chicken spindlin genes on W and Z chromosomes: transcriptional expression of both genes and dynamic behavior of spindlin in interphase and mitotic cells. Chromosome Res. 2001;9(4):283–299. doi: 10.1023/a:1016694513051. [DOI] [PubMed] [Google Scholar]
  23. Kahn N. W., Quinn T. W. Male-driven evolution among Eoaves? A test of the replicative division hypothesis in a heterogametic female (ZW) system. J Mol Evol. 1999 Dec;49(6):750–759. doi: 10.1007/pl00006597. [DOI] [PubMed] [Google Scholar]
  24. Kumar S., Hedges S. B. A molecular timescale for vertebrate evolution. Nature. 1998 Apr 30;392(6679):917–920. doi: 10.1038/31927. [DOI] [PubMed] [Google Scholar]
  25. Lahn B. T., Page D. C. Four evolutionary strata on the human X chromosome. Science. 1999 Oct 29;286(5441):964–967. doi: 10.1126/science.286.5441.964. [DOI] [PubMed] [Google Scholar]
  26. Lahn B. T., Pearson N. M., Jegalian K. The human Y chromosome, in the light of evolution. Nat Rev Genet. 2001 Mar;2(3):207–216. doi: 10.1038/35056058. [DOI] [PubMed] [Google Scholar]
  27. Marshall Graves J. A., Shetty S. Sex from W to Z: evolution of vertebrate sex chromosomes and sex determining genes. J Exp Zool. 2001 Sep 15;290(5):449–462. doi: 10.1002/jez.1088. [DOI] [PubMed] [Google Scholar]
  28. Mindell D. P., Sorenson M. D., Dimcheff D. E., Hasegawa M., Ast J. C., Yuri T. Interordinal relationships of birds and other reptiles based on whole mitochondrial genomes. Syst Biol. 1999 Mar;48(1):138–152. doi: 10.1080/106351599260490. [DOI] [PubMed] [Google Scholar]
  29. Nanda I., Sick C., Münster U., Kaspers B., Schartl M., Staeheli P., Schmid M. Sex chromosome linkage of chicken and duck type I interferon genes: further evidence of evolutionary conservation of the Z chromosome in birds. Chromosoma. 1998 Jun;107(3):204–210. doi: 10.1007/s004120050298. [DOI] [PubMed] [Google Scholar]
  30. Nei M., Gojobori T. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol. 1986 Sep;3(5):418–426. doi: 10.1093/oxfordjournals.molbev.a040410. [DOI] [PubMed] [Google Scholar]
  31. O'Neill M., Binder M., Smith C., Andrews J., Reed K., Smith M., Millar C., Lambert D., Sinclair A. ASW: a gene with conserved avian W-linkage and female specific expression in chick embryonic gonad. Dev Genes Evol. 2000 May;210(5):243–249. doi: 10.1007/s004270050310. [DOI] [PubMed] [Google Scholar]
  32. Ogawa A., Murata K., Mizuno S. The location of Z- and W-linked marker genes and sequence on the homomorphic sex chromosomes of the ostrich and the emu. Proc Natl Acad Sci U S A. 1998 Apr 14;95(8):4415–4418. doi: 10.1073/pnas.95.8.4415. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Posada D., Crandall K. A. MODELTEST: testing the model of DNA substitution. Bioinformatics. 1998;14(9):817–818. doi: 10.1093/bioinformatics/14.9.817. [DOI] [PubMed] [Google Scholar]
  34. Rambaut A., Bromham L. Estimating divergence dates from molecular sequences. Mol Biol Evol. 1998 Apr;15(4):442–448. doi: 10.1093/oxfordjournals.molbev.a025940. [DOI] [PubMed] [Google Scholar]
  35. Saitoh Y., Ogawa A., Hori T., Kunita R., Mizuno S. Identification and localization of two genes on the chicken Z chromosome: implication of evolutionary conservation of the Z chromosome among avian species. Chromosome Res. 1993 Nov;1(4):239–251. doi: 10.1007/BF00710129. [DOI] [PubMed] [Google Scholar]
  36. Schmid M., Enderle E., Schindler D., Schempp W. Chromosome banding and DNA replication patterns in bird karyotypes. Cytogenet Cell Genet. 1989;52(3-4):139–146. doi: 10.1159/000132864. [DOI] [PubMed] [Google Scholar]
  37. Schmid M., Nanda I., Guttenbach M., Steinlein C., Hoehn M., Schartl M., Haaf T., Weigend S., Fries R., Buerstedde J. M. First report on chicken genes and chromosomes 2000. Cytogenet Cell Genet. 2000;90(3-4):169–218. doi: 10.1159/000056772. [DOI] [PubMed] [Google Scholar]
  38. Searle A. G., Peters J., Lyon M. F., Hall J. G., Evans E. P., Edwards J. H., Buckle V. J. Chromosome maps of man and mouse. IV. Ann Hum Genet. 1989 May;53(Pt 2):89–140. doi: 10.1111/j.1469-1809.1989.tb01777.x. [DOI] [PubMed] [Google Scholar]
  39. Shetty S., Griffin D. K., Graves J. A. Comparative painting reveals strong chromosome homology over 80 million years of bird evolution. Chromosome Res. 1999;7(4):289–295. doi: 10.1023/a:1009278914829. [DOI] [PubMed] [Google Scholar]
  40. Waddell P. J., Cao Y., Hasegawa M., Mindell D. P. Assessing the Cretaceous superordinal divergence times within birds and placental mammals by using whole mitochondrial protein sequences and an extended statistical framework. Syst Biol. 1999 Mar;48(1):119–137. doi: 10.1080/106351599260481. [DOI] [PubMed] [Google Scholar]
  41. Watson J. M., Spencer J. A., Riggs A. D., Graves J. A. Sex chromosome evolution: platypus gene mapping suggests that part of the human X chromosome was originally autosomal. Proc Natl Acad Sci U S A. 1991 Dec 15;88(24):11256–11260. doi: 10.1073/pnas.88.24.11256. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Yen P. H., Marsh B., Allen E., Tsai S. P., Ellison J., Connolly L., Neiswanger K., Shapiro L. J. The human X-linked steroid sulfatase gene and a Y-encoded pseudogene: evidence for an inversion of the Y chromosome during primate evolution. Cell. 1988 Dec 23;55(6):1123–1135. doi: 10.1016/0092-8674(88)90257-7. [DOI] [PubMed] [Google Scholar]
  43. de Kloet S. R. Loss of the gene for the alpha subunit of ATP synthase (ATP5A1) from the W chromosome in the African grey parrot (Psittacus erithacus). J Mol Evol. 2001 Aug;53(2):135–143. doi: 10.1007/s002390010201. [DOI] [PubMed] [Google Scholar]
  44. van Tuinen M., Hedges S. B. Calibration of avian molecular clocks. Mol Biol Evol. 2001 Feb;18(2):206–213. doi: 10.1093/oxfordjournals.molbev.a003794. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES