Skip to main content
SpringerLink
Log in

Common Mechanisms of Y Chromosome Evolution

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

Y chromosome evolution is characterized by the expansion of genetic inertness along the Y chromosome and changes in the chromosome structure, especially the tendency of becoming heterochromatic. It is generally assumed that the sex chromosome pair has developed from a pair of homologues. In an evolutionary process the proto-Y-chromosome, with a very short differential segment, develops in its final stage into a completely heterochromatic and to a great extends genetically eroded Y chromosome. The constraints evolving the Y chromosome have been the objects of speculation since the discovery of sex chromosomes. Several models have been suggested. We use the exceptional situation of the in Drosophila mirandato analyze the molecular process in progress involved in Y chromosome evolution. We suggest that the first steps in the switch from a euchromatic proto-Y-chromosome into a completely heterochromatic Y chromosome are driven by the accumulation of transposable elements, especially retrotransposons inserted along the evolving nonrecombining part of the Y chromosome. In this evolutionary process trapping and accumulation of retrotransposons on the proto-Y-chromosome should lead to conformational changes that are responsible for successive silencing of euchromatic genes, both intact or already mutated ones and eventually transform functionally euchromatic domains into genetically inert heterochromatin. Accumulation of further mutations, deletions, and duplications followed by the evolution and expansion of tandem repetitive sequence motifs of high copy number (satellite sequences) together with a few vital genes for male fertility will then represent the final state of the degenerated Y chromosome.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Barrio, E., A. Latorre, A. Moya & F.J. Ayala, 1992. Phylogenetic reconstruction of the Drosophila obscuragroup, on the basis of mitochondrial DNA. Mol. Biol. Evol. 9: 621–635.

    PubMed  CAS  Google Scholar 

  • Beverly, S.M. & A.C. Wilson, 1984. Molecular evolution in Drosophilaand the higher Diptera II. A time scale for fly evolution. J. Mol. Evol. 21: 1–23.

    Article  Google Scholar 

  • Bonaccorsi, S., C. Pisano, F. Puoti & M. Gatti, 1988. Y chromosome loops in Drosophila melanogaster. Genetics 120: 1015–1034.

    PubMed  CAS  Google Scholar 

  • Bridges, C.B., 1916a. Non-disjunction as proof of the chromosome theory of heredity. Genetics 1: 1–52.

    PubMed  CAS  Google Scholar 

  • Bridges, C.B., 1916b. Non-disjunction as proof of the chromosome theory of heredity. Genetics 1: 107–163.

    PubMed  CAS  Google Scholar 

  • Bull, J.J., 1983. Evolution of Sex Determining Mechanisms, Benjamin/ Cummings, Menlo Park, CA, pp. 248–269.

    Google Scholar 

  • Burgoyne, P.S., 1998. The mammalian Y chromosome: a new perspective. BioEssays 20: 363–366.

    Article  PubMed  CAS  Google Scholar 

  • Charlesworth, B., 1978. A model for the evolution of Y chromosomes and dosage compensation. Proc. Natl. Acad. Sci. USA 75: 5618–5622.

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Charlesworth, B., 1996. The evolution of chromosomal sex determination and dosage compensation. Current Biology 6: 149–162.

    Article  PubMed  CAS  Google Scholar 

  • Charlesworth, B., D. Charlesworth, J. Hnilicka, A. Yu & D.S. Guttman, 1997. Lack of degeneration loci on the neo-Ychromosome of Drosophila americana americana. Genetics 145: 989–1002.

    PubMed  CAS  Google Scholar 

  • Dobzhansky, Th., 1935. Drosophila miranda, a new species. Genetics 20: 377–391.

    PubMed  CAS  Google Scholar 

  • Eichler, E.E., 1998. Masquarading repeats: paralogous pitfalls of the human genome. Genome Res. 8: 758–762.

    PubMed  CAS  Google Scholar 

  • Fridolfsson, A.-K., H. Cheng, G.N. Copeland, N.A. Jenkins, H.-C. Liu, T. Raudsepp, T. Woodage, B. Chowdhary, 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.

    Article  PubMed  CAS  Google Scholar 

  • Gatti, M. & S. Pimpinelli, 1983. Cytological and genetic analysis of the Y chromosome of Drosophila melanogaster: I. Organization of the fertility factors. Chromosoma 88: 349–373.

    Article  Google Scholar 

  • Gatti, M. & S. Pimpinelli, 1992. Functional elements in Drosophila melanogasterheterochromatin. Annu. Rev. Genet. 26: 239–275.

    Article  PubMed  CAS  Google Scholar 

  • Gepner, J. & T.S. Hays, 1993. A fertility region on the Y chromosome of Drosophila melanogasterencodes a dynein microtubule motor. Proc. Natl. Acad. Sci. USA 90: 11132–11136.

    Article  PubMed  CAS  Google Scholar 

  • Graves, J.A.M., 1995. The origin and function of the mammalian Y chromosome and Y-borne genes – an evolving understanding. BioEssays 17: 311–320.

    Article  PubMed  CAS  Google Scholar 

  • Graves, J.A.M., 1996. Mammals that break the rules: genetics of marsupials and monotremes. Annu. Rev. Genet. 30: 233–260.

    Article  PubMed  CAS  Google Scholar 

  • Graves, J.A.M., C.M. Disteche & R. Toder, 1998. Gene dosage in the evolution and function of mammalian sex chromosomes. Cytogenet. Cell Genet. 80: 94–103.

    CAS  Google Scholar 

  • Hackstein, J.H.P., 1987. Spermatogenesis in Drosophila hydei, pp. 63–116 in Results and Problems in Cell Differentiation (Spermatogenesis: Genetic Aspects, Vol. 15), edited by W. Hennig, Springer-Verlag, Berlin.

    Google Scholar 

  • Hackstein, J.H.P. & R. Hochstenbach, 1995. The elusive fertility genes of Drosophila: the ultimate haven for selfish genetic elements. Trends Genet. 11: 195–200.

    Article  PubMed  CAS  Google Scholar 

  • Hardy, R.W., K.T. Tokuyasu & D.L. Lindsley, 1981. Analysis of spermatogenesis in Drosophila melanogasterbearing deletions for Y-chromosome fertillity genes. Chromosoma 88: 593–617.

    Article  Google Scholar 

  • Hess, O., 1967. Complementation of genetic activities in translocated fragments of the Y chromosome in Drosophila hydei. Genetics 56: 283–295.

    PubMed  CAS  Google Scholar 

  • Kumar, S. & S.B. Hedges, 1998. A molecular timescale for vertebrate evolution. Nature 392: 917–920.

    Article  PubMed  CAS  Google Scholar 

  • Kurek, R., A.M. Reugels, K.H. Glätzer & H. Bünemann, 1998. The Y chromosomal fertility factor Threads in Drosophila hydeiharbors a functional gene encoding an axonemal dynein b heavy chain protein. Genetics 149: 1363–1376.

    PubMed  CAS  Google Scholar 

  • Labrador, M. & V.G. Corces, 1997. Transposable element–host interactions: regulation of insertion and excision. Annu. Rev. Genet. 31: 381–404.

    Article  PubMed  CAS  Google Scholar 

  • Lahn, B.T. & D.C. Page, 1997. Functional coherence of the human Y chromosome. Science 278: 675–680.

    Article  PubMed  CAS  Google Scholar 

  • Lahn, B.T. & D.C. Page, 1999. Four evolutionary strata on the human X chromosome. Science 286: 964–967.

    Article  PubMed  CAS  Google Scholar 

  • Lohe, A.R. & A.J. Hilliker, 1995. Return of the H-word (heterochromatin). Curr. Opin. Genet. Dev. 5: 746–755.

    Article  PubMed  CAS  Google Scholar 

  • Lucchesi, J.C., 1978. Gene dosage compensation and the evolution of sex chromosomes. Science 202: 711–716.

    PubMed  CAS  Google Scholar 

  • Lucchesi, J.C., 1994. The evolution of heteromorphic sex chromosomes. BioEssays 16: 81–83.

    Article  PubMed  CAS  Google Scholar 

  • Lucchesi, J.C., 1996. Dosage compensation in Drosophilaand the ‘complex’ world of transcriptional regulation. BioEssays 18: 541–547.

    Article  PubMed  CAS  Google Scholar 

  • MacKnight, R.H., 1939. The sex-determining mechanism of Drosophila miranda. Genetics 24: 180–201.

    PubMed  CAS  Google Scholar 

  • Marsh, J.L. & E. Wieschaus, 1978. Is sex determination in germ line and soma controlled by separate genetic mechanisms? Nature 272: 249–251.

    Article  PubMed  CAS  Google Scholar 

  • McAllister, B.F. & B. Charlesworth, 1999. Reduced sequence variability on the neo-Ychromosome of Drosophila americana americana. Genetics 153: 221–233.

    PubMed  CAS  Google Scholar 

  • Muller, H.J., 1918. Genetic variability, twin hybrids and constant hybrids, a case of balanced lethal factors. Genetics 3: 422–499.

    PubMed  CAS  Google Scholar 

  • Muller, H.J., 1932. Some genetic aspects of sex. Am. Nat. 66: 118–138.

    Article  Google Scholar 

  • Muller, H.J., 1940. Bearings of the Drosophilawork on systematics pp. 185–268 in The New Systematics edited by I. Huxley. Oxford University Press, Oxford.

    Google Scholar 

  • Ohno, S. 1967. Sex chromosomes and Sex-Linked Genes. Springer, Berlin.

    Google Scholar 

  • Pimpinelli, S., M. Berloco, L. Fanti, P. Dimitri, S. Bonaccorsi, E. Marchetti, R. Caizzi, C. Caggese & M. Gatti, 1995. Transposable elements are stable structural component of Drosophila melanogasterheterochromatin. Proc. Natl. Acad. Sci. USA 92: 3804–3808.

    Article  PubMed  CAS  Google Scholar 

  • Rice, W.R., 1987. Genetic hitchhiking and the evolution of reduced genetic activity of the Y sex chromosome. Genetics 116: 161–167.

    PubMed  CAS  Google Scholar 

  • Rice, W.R., 1994. Degeneration of a non-recombining chromosome. Science 263: 230–232.

    PubMed  CAS  Google Scholar 

  • Rice, W. R., 1996. Evolution of the Y sex chromosome in animals. BioScience 46: 331–343.

    Article  Google Scholar 

  • Russo, C.A.M., N. Takezaki & M. Nei, 1995. Molecular phylogeny and divergence times of Drosophilid species. Mol. Biol. Evol. 12: 391–404.

    PubMed  CAS  Google Scholar 

  • Sharman, G., R. Hughes & D. Cooper, 1990. The chromosomal basis of sex differentiation in marsupials. Aust. J. Zool. 37: 451–466.

    Article  Google Scholar 

  • Spradling, A.C., 1994. Transposable elements and the evolution of heterochromatin, pp. 69–83 in Molecular Evolution of Physiological Processes, edited by D. Fambrough. Rockefeller University Press, New York.

    Google Scholar 

  • Steinemann, M., 1982. Multiple sex chromosomes in Drosophila miranda: A system to study the degeneration of a chromosome. Chromosoma 86: 59–76.

    Article  PubMed  CAS  Google Scholar 

  • Steinemann, M. & S. Steinemann, 1992. Degenerating Y chromosome of Drosophila miranda: A trap for retrotransposons. Proc. Natl. Acad. Sci. USA 89: 7591–7595.

    Article  PubMed  CAS  Google Scholar 

  • Steinemann, M. & S. Steinemann, 1993. A duplication including the Yallele of Lcp2and the TRIMretrotransposon at the Lcplocus on the degenerating neo-Ychromosome of Drosophila miranda: Molecular structure and mechanisms by which it may have arisen. Genetics 134: 497–505.

    PubMed  CAS  Google Scholar 

  • Steinemann, M., S. Steinemann & F. Lottspeich, 1993. How Y chromosomes become genetically inert. Proc. Natl. Acad. Sci. USA 90: 5737–5741.

    Article  PubMed  CAS  Google Scholar 

  • Steinemann, M., S. Steinemann & B. M. Turner, 1996. Evolution of dosage compensation. Chromosome Res. 4: 185–190.

    Article  PubMed  CAS  Google Scholar 

  • Steinemann, M. & S. Steinemann, 1998. Enigma of Ychromosome degeneration: Neo-Yand Neo-Xchromosomes of Drosophila mirandaa model for sex chromosome evolution. Genetica 102/103: 409–420.

    Article  CAS  Google Scholar 

  • Steinemann, S. & M. Steinemann, 1999. The Amylasegene cluster on the evolving sex chromosomes of Drosophila miranda. Genetics 151: 151–161.

    PubMed  CAS  Google Scholar 

  • Throckmorton, L.H., 1982. The virilisspecies group, pp. 227–296 in The Genetics and Biology of Drosophila, edited by M. Ashburner, H.L. Carson & J.N. Thomson. Academic Press, London.

    Google Scholar 

  • Tomlinson, I., G. Cook, N. Carter, R. Elaswarapu, S. Smith, G. Walter, L. Buluwela, T. Rabbitts & G. Winter, 1994. Human immunglobulin VH and D segments on chromosomes 15q11.2 and 16p11.2. Hum. Mol. Genet. 3: 853–860.

    PubMed  CAS  Google Scholar 

  • Vogt, P.H., N. Affara, P. Davey, M. Hammer, M.A. Jobling, Y.-F.C. Lau, M. Mitchell, W. Schempp, C. Tyler-Smith, G. Williams, P. Yen & G.A. Rappold, 1997. Report of the third international workshop on human Ychromosome mapping. Cytogenet. Cell Genet. 79: 1–20.

    Article  PubMed  CAS  Google Scholar 

  • Zhang, P. & R.L. Stankiewicz, 1998. Y-linked male sterile mutations induced by P element in Drosophila melanogaster. Genetics 150: 735–744.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institut für Zoologie, Technische Universität Darmstadt, Schnittspahnstr. 3, D-64287, Darmstadt, FR, Germany

    Manfred Steinemann & Sigrid Steinemann

Authors
  1. Manfred Steinemann
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sigrid Steinemann
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Steinemann, M., Steinemann, S. Common Mechanisms of Y Chromosome Evolution. Genetica 109, 105–111 (2000). https://doi.org/10.1023/A:1026584016524

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1026584016524

Search

Navigation