Skip to main content
Log in

Evolution of the Spindlin Gene in Birds: Independent Cessation of the Recombination of Sex Chromosomes at the Spindlin Locus in Neognathous Birds and Tinamous, a Palaeognathous Avian Family

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

Tinamous (Aves, Palaeognathae, Tinamiformes) are primitive birds, generally considered to be the sister group to the ratites. Tinamous possess a W sex-chromosome, intermediate in heterochromatization between the largely euchromatic W chromosome of the ratites and the highly condensed W chromosome of the neognathous birds. Of the four genes which are known to have diverged copies on the neognathous avian W and Z chromosome (ATP5A1, CHD1, PKC and SPIN) only the spindlin gene has W- and Z-chromosomal forms in the tinamiformes. This paper describes experiments which show that the sequences of these forms are more similar to each other and to the homologous undifferentiated spindlin gene sequences in the ratite genome than to the W or Z forms of the spindlin gene in other, neognathous species. This suggests that cessation of recombination at the spindlin locus of the ancestral W and Z chromosomes of the paleognathous tinamiformes and the neognathous avian species were independent events.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Ansart, H.A., N. Takagi & M. Sasaki, 1988. Morphological differentiation of sex chromosomes in three species of ratite birds. Cytogenet. Cell Genet. 47: 185–188.

    Google Scholar 

  • Barnes, W.M., 1994. PCR amplification of up to 35-kb DNA with high fidelity and high yield from lambda bacteriophage templates. Proc. Natl. Acad. Sci. USA 91: 2216–2220.

    PubMed  Google Scholar 

  • Blanck, A., B. Gluck, Wartbichler, S. Bender, M. Poll & A. Brandl, 1997. Activity of restriction enzymes in a PCR mix. Biochemica (Boehringer) 3: 25.

    Google Scholar 

  • Bull, J.J., 1983. Evolution of Sex Determining Mechanisms. Benjamin/Cummings, Menlo Park, CA.

    Google Scholar 

  • Burch, J.B.E., D.L. Davis & N.B. Haas, 1993. Chicken repeat 1 elements contain a pol-like open reading frame and belong to the non-long terminal repeat class of retroposons. Proc. Natl. Acad. Sci. USA 90: 8199–8203.

    PubMed  Google Scholar 

  • Caspers, G.J., J. Wattel & W.W. de Jong, 1994. Alpha A-crystallin sequences group tinamou with ratites. Mol. Biol. Evol. 11: 711–713.

    PubMed  Google Scholar 

  • Charlesworth, B., 1991. The evolution of sex chromosomes. Science 251: 1030–1033.

    PubMed  Google Scholar 

  • Cooper, A. & D. Penny, 1997. Mass survival of birds across the cretaceous-tertiary boundary: molecular evidence. Science 275: 1109–1113.

    PubMed  Google Scholar 

  • Cooper, A., C. Laluesa-Fox, S. Anderson A. Rambaut, J. Austin & R. Ward, 2001. Complete mitochondrial genome sequences of two extinct moas clarify ratite evolution. Nature 409: 704–707.

    PubMed  Google Scholar 

  • Cracraft, J. & D.P. Mindell, 1989. The early history of modern birds: a comparison of molecular and morphological evidence, pp 389–403 in The Hierarchy of Life, edited by B. Fernholm, K. Brenner & H. Jornvall. Elsevier, Amsterdam.

    Google Scholar 

  • de Kloet, S.R., 2001a. Loss of the gene for the alpha subunit of ATP synthase (ATP5W1) from theWchromosome of the African grey parrot (Psittacus eritacus). J. Mol. Evol. 53: 135–143.

    PubMed  Google Scholar 

  • de Kloet, S.R., 2001b. Development of a CAPS (Cleaved Amplified Polymorphics Sequence) assay for sex identification of the emu (Dromaius novaehollandiae). Mol. Ecol. Notes 1: 273–275.

    Google Scholar 

  • de Kloet, S.R., 2002. Molecular sex identification of tinamous with PCR using primers derived from the spindlin gene. Mol. Ecol. Notes 2: 465–466.

    Google Scholar 

  • Dvorak, J., J.L. Halverson, P. Gulick, K.A. Rauen, U.K. Abbott, B.J. Kelly & F.T. Schultz, 1992. cDNA cloning of a Z-and W-linked gene in gallinaceous birds. J. Hered. 83: 22–25.

    Google Scholar 

  • Edwards, S.V., B. Fertil, A. Giron & P.J. Deschavanne, 2001. A genomic schism in birds revealed by phylogenetic analysis of DNA strings. Syst. Biol. 51: 599–613.

    Google Scholar 

  • Ellegren, H., 1996. First gene on the avian Wchromosome (CHD1) provides a tag for universal sexing of non-ratite birds. Proc. R. Soc. London Ser. B. 1377: 1635–1641.

    Google Scholar 

  • Ellegren, H., 2000. Evolution of the avian sex chromosomes and their role in sex determination. Trends Ecol. 15: 188–192.

    Google Scholar 

  • Ellegren, H. & A. Carmichael, 2001. Multiple and independent cessation of recombination between avian sex chromosomes. Genetics 158: 325–331.

    PubMed  Google Scholar 

  • Fridolfsson, A.-K., H.H. Cheng, N.G. Copeland, N.A. Jenkins, H.C. Liu, T. Raudseep, T.M. Woodage, B. Chowdary, J. Halverson & H. Ellegren, 1998. Evolution of the avian sex chromosomes from an ancestral pair of autosomes. Proc. Natl. Acad. Sci. USA 95: 8147–8152.

    PubMed  Google Scholar 

  • Garcia-Moreno, J. & D.P. Mindell, 2000. Rooting a phylogeny with homologous genes on opposite sex chromosomes (gametologs): a case study using avian CHD. Mol. Biol. Evol. 17: 1826–1832.

    PubMed  Google Scholar 

  • Grantham, R., 1974. Amino acid difference formula to help explain protein evolution. Science 185: 862–864.

    PubMed  Google Scholar 

  • Griffiths, R., S. Daan & C. Dijkstra, 1996. Sex identification in birds using two CHD1 genes. Proc. R. Soc. London Ser. B. 1374: 1251–1256.

    Google Scholar 

  • Griffiths, R., M.C. Double, K. Or & R.J.G. Dawson, 1998. A DNA test to sex most birds. Mol. Ecol. 7: 1071–1075.

    PubMed  Google Scholar 

  • Gustincich, S., G. Manfioletti, C. Del Sal, C. Schneider & P.C. Carnici, 1991. A fast method for high-quality genomic DNA extraction from whole human blood. Biotechniques 11: 298–302.

    PubMed  Google Scholar 

  • Haddrath, O. & A.J. Baker, 2001. Complete mitochondrial DNA genome sequences of extinct birds: ratite phylogenetics and the vicariance biogeography hypothesis. Proc. R. Soc. London Ser. B. 268: 939–945.

    Google Scholar 

  • Hedges, S.B., 1994. Molecular evidence for the origin of birds. Proc. Natl. Acad. Sci. USA 91: 2621–2624.

    PubMed  Google Scholar 

  • Hedges, S.B. & L.L. Poling, 1999. A molecular phylogeny of reptiles. Science 283: 998–1001.

    PubMed  Google Scholar 

  • Hoppe, B.L., B.M. Conti-Tronconi & R.M. Horton, 1992. Gelloading dyes compatible with PCR. Biotechniques 12: 679–680.

    PubMed  Google Scholar 

  • Hori, T., S. Asakawa, Y. Itoh, N. Shimizu & S. Mizuno, 2000. Wpkc1, 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 early female sex determination. Mol. Biol. Cell 11: 3645–3660.

    PubMed  Google Scholar 

  • Huynen L., C.D. Millar & D.M. Lambert, 2002. A DNA test to sex ratite birds. Mol. Ecol. 11: 851–856.

    PubMed  Google Scholar 

  • Itoh, Y., T. Hori, H. Saitoh & S. Mizuno, 2001a. 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. 9: 283–299.

    PubMed  Google Scholar 

  • Itoh, Y., M. Suzuki, A. Ogawa, I. Munechika, K. Murata & S. Mizuno, 2001b. Identification of the sex of a wide range of Carinatae birds by PCR using primer sets selected from chicken EEO.6 and its related sequences. J. Hered. 92: 315–321.

    PubMed  Google Scholar 

  • Malik, H.S. & T.H. Eickbush, 1998. The RTE class of non-LTR retroposons is widely distributed in animals and is the origin of many SINEs. Mol. Biol. Evol. 15: 1123–1134.

    PubMed  Google Scholar 

  • Maniatis, T., E.F. Fritsch & J. Sambrook, 1983. Molecular Cloning; A Laboratory Manual. Cold Spring Harbour Laboratory. Cold Spring Harbour, New York.

    Google Scholar 

  • Menossi, M., N. Cremonese, L.G. Maron & P. Arruda, 2000. Making colony PCR easier by adding gel-loading buffer to the amplification reaction. Biotechniques 28: 424–426.

    PubMed  Google Scholar 

  • Ogawa, A., I. Solovei, N. Hutchison, Y. Saitoh, J. Ikeda, H. MacGregor & S. Mizuno, 1997. Molecular characterization and cytological mapping of a non-repetitive DNA sequence region from the W chromosome of chicken and its use as a universal probe for sexing carinate birds. Chromosome Res. 5: 93–101.

    PubMed  Google Scholar 

  • Ohno, S., 1967. Sex Chromosomes and Sex-linked Genes. Springer, Berlin.

    Google Scholar 

  • O'Neill, M., M. Binder, C. Smith, J. Andrews, K. Reed, M. Smith, C. Millar, D. Lambert & A. Sinclair, 2000. ASW: a gene with conserved avian W-linkage and female specific expression in chick embryonic gonad. Dev. Genes Evol. 219: 243–249.

    Google Scholar 

  • Parry, H.D. & L. Alphey, 1995. The utilization of cloned DNAs. in DNA Cloning: 1 Core Techniques, edited by D.M. Glover & B.D. Hames. Oxford University Press, Oxford.

    Google Scholar 

  • Pigozzi, M.I. & A.J. Solari, 1997. Extreme axial equalization and wide distribution of recombination nodules in the primitive ZW pair of Rhea americana (Aves, Ratitae). Chromosome Res. 5: 421–428.

    PubMed  Google Scholar 

  • Pigozzi, M.I. & A.J. Solari, 1999. The ZW pairs of two paleognath birds from two orders show transitional W chromosome differentiation. Chromosome Res. 7: 541–551.

    PubMed  Google Scholar 

  • Sanger, F., S. Nicklen & A.R. Coulson, 1977. DNA sequencing with chain terminating inhibitors. Proc. Natl. Acad. Sci. USA 74: 5463–5467.

    PubMed  Google Scholar 

  • Swofford, D.L., 1998. PAUP: Phylogenetic Analysis Using Parsimony. Version 4.0 b2. Sinauer, Sunderland, MA, USA.

    Google Scholar 

  • Tajima, E. & M. Nei. 1984. Estimation of evolutionary distance between nucleotide sequences. Mol. Biol. Evol. 1: 269–285.

    PubMed  Google Scholar 

  • Thompsson, J.D., T.J. Gibson, F. Plewniak, F. Jeanmougin & D.G. Higgins, 1997. The ClustalX interface: flexible strategies for multiple sequence alignment aide by quality analysis tools. Nucleic Acids Res. 25: 4876–4882.

    Article  PubMed  Google Scholar 

  • Van Tuinen, M. & S.B. Hedges, 2001. Calibration of avian molecular clocks. Mol. Biol. Evol. 18: 206–213.

    PubMed  Google Scholar 

  • Van Tuinen, M., G.C. Sibley & S.B. Hedges, 1998. Phylogeny and biogeography of ratite birds inferred from DNA sequences of the mitochondrial ribosomal genes. Mol. Biol. Evol. 15: 370–376.

    PubMed  Google Scholar 

  • Vondergon, T.L. & M. Reitman, 1994. Evolution of chicken repeat 1 (CR1) elements: evidence for ancient subfamilies and multiple progenitors. Mol. Biol. Evol. 11: 886–898.

    PubMed  Google Scholar 

  • Zon, L.I., D.M. Durfman & S.H. Orkin, 1991. The polymerase chain reaction miniprep. Biotechniques 7: 696–698.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to S.R. de Kloet.

Rights and permissions

Reprints and permissions

About this article

Cite this article

de Kloet, R., de Kloet, S. Evolution of the Spindlin Gene in Birds: Independent Cessation of the Recombination of Sex Chromosomes at the Spindlin Locus in Neognathous Birds and Tinamous, a Palaeognathous Avian Family. Genetica 119, 333–342 (2003). https://doi.org/10.1023/B:GENE.0000003842.72339.df

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/B:GENE.0000003842.72339.df

Navigation