Skip to main content
SpringerLink
Log in

Non-homologous sex chromosomes of birds and snakes share repetitive sequences

  • Published:
Chromosome Research Aims and scope Submit manuscript

Abstract

Snake sex chromosomes provided Susumo Ohno with the material on which he based his theory of how sex chromosomes differentiate from autosomal pairs. Like birds, snakes have a ZZ male/ZW female sex chromosome system, in which the snake Z is a macrochromosome much the same size as the bird Z. However, the gene content shows clearly that the snake and bird Z chromosomes are completely non-homologous. The molecular aspect of W chromosome degeneration in snakes remains largely unexplored. We used comparative genomic hybridization to identify the female-specific region of the W chromosome in representative species of Australian snakes. Using this approach, we show that an increasingly complex suite of repeats accompanies the evolution of W chromosome heteromorphy. In particular, we found that while the python Liasis fuscus exhibits no sex-specific repeats and indeed, no cytologically recognizable sex-specific region, the colubrid Stegonotus cucullatus shows a large domain on the short arm of the W chromosome that consists of female-specific repeats, and the large W of Notechis scutatus is composed almost entirely of repetitive sequences, including Bkm and 18S rDNA-related elements. FISH mapping of both simple and complex probes shows patterns of repeat amplification concordant with the size of the female-specific region in each species examined. Mapping of intronic sequences of genes that are sex-linked in both birds (DMRT1) and snakes (CTNNB1) reveals massive amplification in discrete domains on the W chromosome of the elapid N. scutatus. Using chicken W chromosome paint, we demonstrate that repetitive sequences are shared between the sex chromosomes of birds and derived snakes. This could be explained by ancestral but as yet undetected shared synteny of bird and snake sex chromosomes or may indicate functional homology of the repeats and suggests that degeneration is a convergent property of sex chromosome evolution. We also establish that synteny of snake Z-linked genes has been conserved for at least 166 million years and that the snake Z consists of two conserved blocks derived from the same ancestral vertebrate 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

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

BAC:

Bacterial artificial chromosome

Bkm:

Banded krait minor satellite DNA

CGH:

Comparative genomic hybridization

DAPI:

4′,6-diamidino-2-phenylindole

DOP-PCR:

Degenerate oligonucleotide primed polymerase chain reaction

dUTP:

2′-deoxyuridine 5′-triphosphate

FISH:

Fluorescence in-situ hybridization

GGA:

Gallus gallus

HSA:

Homo sapiens

MSY:

Male-specific region on the Y chromosome

MYA:

Million years ago

NOR:

Nucleolus organizer region

PCR:

Polymerase chain reaction

rDNA:

Ribosomal DNA

SSC:

Standard saline citrate

v/v:

Volume/volume

w/v:

Weight/volume

XTR:

Xenopus tropicalis

References

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    CAS  PubMed  Google Scholar 

  • Arnemann J, Jakubiczka S, Schmidtke J, Schäfer R, Epplen JT (1986) Clustered GATA repeats (Bkm sequences) on the human Y chromosome. Hum Genet 73:301–303

    Article  CAS  PubMed  Google Scholar 

  • Beçak W, Beçak ML, Nazareth HRS, Ohno S (1964) Close karyological kinship between the reptilian suborder Serpentes and the class Aves. Chromosoma 15:606–617

    Article  PubMed  Google Scholar 

  • Bianchi NO, Beçak W, Bianchi MSA, Beçak ML, Rabello MN (1969) Chromosome replication in four species of snakes. Chromosoma 26:188–200

    Article  CAS  PubMed  Google Scholar 

  • Brunner B et al (2001) Genomic organization and expression of the doublesex-related gene cluster in vertebrates and detection of putative regulatory regions for DMRT1. Genomics 77:8–17

    Article  CAS  PubMed  Google Scholar 

  • Bull JJ (1983) Evolution of sex determining mechanisms. Benjamin/Cummings, San Francisco

    Google Scholar 

  • Charlesworth D, Charlesworth B (1980) Sex differences in fitness and selection for centric fusions between sex-chromosomes and autosomes. Genet Res 35:205–214

    Article  CAS  PubMed  Google Scholar 

  • Charlesworth B, Sniegowski P, Stephan W (1994) The evolutionary dynamics of repetitive DNA in eukaryotes. Nature 371:215–220

    Article  CAS  PubMed  Google Scholar 

  • Charlesworth D, Charlesworth B, Marais G (2005) Steps in the evolution of heteromorphic sex chromosomes. Heredity 95:118–128

    Article  CAS  PubMed  Google Scholar 

  • Epplen JT (1988) On simple repeated GATCA sequences in animal genomes: a critical reappraisal. J Hered 79:409

    CAS  PubMed  Google Scholar 

  • Epplen JT, McCarrey JR, Sutou S, Ohno S (1982) Base sequence of a cloned snake W-chromosome DNA fragment and identification of a male-specific putative mRNA in the mouse. Proc Natl Acad Sci 79:3798–3802

    Article  CAS  PubMed  Google Scholar 

  • Epplen JT, Cellini A, Shorte M, Ohno S (1983) On evolutionarily conserved simple repetitive DNA sequences: do “sex-specific” satellite components serve any sequence dependent function? Differ Res Biol Divers 23 Suppl:S60–S63

    Google Scholar 

  • Ezaz T, Quinn AE, Miura I, Sarre SD, Georges A, Graves JAM (2005) The dragon lizard Pogona vitticeps has ZZ/ZW micro-sex chromosomes. Chromosome Res 13:763–776

    Article  CAS  PubMed  Google Scholar 

  • Ezaz T, Quinn AE, Sarre SD, O’Meally D, Georges A, Marshall GJA (2009a) Molecular marker suggests rapid changes of sex-determining mechanisms in Australian dragon lizards. Chromosome Res 17:91–98

    Article  CAS  PubMed  Google Scholar 

  • Ezaz T, Moritz B, Waters P, Graves JAM, Georges A, Sarre SD (2009b) The ZW sex microchromosomes of an Australian dragon lizard share no homology with those of other reptiles or birds. Chromosome Res 17:965–973

    Article  CAS  PubMed  Google Scholar 

  • Fisher RA (1931) The evolution of dominance. Biol Rev 6:345–368

    Article  Google Scholar 

  • Gall JG (1968) Differential synthesis of the genes for ribosomal RNA during amphibian oogenesis. Proc Natl Acad Sci USA 60:553–560

    Article  CAS  PubMed  Google Scholar 

  • Glas R, Graves JAM, Toder R, Ferguson-Smith M, O’Brien PC (1999) Cross-species chromosome painting between human and marsupial directly demonstrates the ancient region of the mammalian X. Mamm Genome 10:1115–1116

    Article  CAS  PubMed  Google Scholar 

  • Graves JAM (1998) Evolution of the mammalian Y chromosome and sex-determining genes. J Exp Zool 281:5

    Article  Google Scholar 

  • Graves JAM (2006) Sex chromosome specialization and degeneration in mammals. Cell 124:901–914

    Article  PubMed  Google Scholar 

  • Graves JAM, Shetty S (2001) Sex from W to Z: evolution of vertebrate sex chromosomes and sex determining genes. J Exp Zool 290(5):449–62

    Article  Google Scholar 

  • Griffin DK et al (1999) Micro-and macrochromosome paints generated by flow cytometry and microdissection: tools for mapping the chicken genome. Cytogenet Cell Genet 87:278–281

    Article  CAS  PubMed  Google Scholar 

  • Griffiths R, Holland PWH (1990) A novel avian W chromosome DNA repeat sequence in the lesser black-backed gull (Larus fuscus). Chromosoma 99:243–250

    Article  CAS  PubMed  Google Scholar 

  • Haines H (2005) How do male kangaroos cope with only half as many ribosomal RNA genes as female kangaroos. Honours Thesis. Australian National University, Canberra

  • Hays WL (1994) Statistics, 5th edn. Harcourt Brace, New York

    Google Scholar 

  • Hedges SB, Dudley J, Kumar S (2006) TimeTree: a public knowledge-base of divergence times among organisms. Bioinformatics 22:2971–2972

    Article  CAS  PubMed  Google Scholar 

  • Hellsten U et al (2010) The genome of the Western Clawed Frog Xenopus tropicalis. Science 328:633–636

    Article  CAS  PubMed  Google Scholar 

  • Hughes JF et al (2010) Chimpanzee and human Y chromosomes are remarkably divergent in structure and gene content. Nature 463:536–539

    Article  CAS  PubMed  Google Scholar 

  • Itoh Y, Mizuno S (2002) Molecular and cytological characterization of SspI-family repetitive sequence on the chicken W chromosome. Chromosome Res 10:499–511

    Article  CAS  PubMed  Google Scholar 

  • Itoh Y, Kampf K, Arnold A (2008) Molecular cloning of zebra finch W chromosome repetitive sequences: evolution of the avian W chromosome. Chromosoma 117:111–121

    Article  CAS  PubMed  Google Scholar 

  • Jones KW, Singh L (1981) Conserved repeated DNA sequences in vertebrate sex chromosomes. Hum Genet 58:46–53

    Article  CAS  PubMed  Google Scholar 

  • Jones K, Singh L (1985) Snakes and the evolution of sex chromosomes. Trends Genet 1:55–61

    Article  Google Scholar 

  • Kawai A, Nishida-Umehara C, Ishijima J, Tsuda Y, Ota H, Matsuda Y (2007) Different origins of bird and reptile sex chromosomes inferred from comparative mapping of chicken Z-linked genes. Cytogenet Genome Res 117:92–102

    Article  CAS  PubMed  Google Scholar 

  • Kirpichnikov VS (1981) Genetic bases of fish selection. Springer, New York

    Google Scholar 

  • Kodama H, Saitoh H, Tone M, Kuhara S, Sakaki Y, Mizuno S (1987) Nucleotide sequences and unusual electrophoretic behavior of the W chromosome-specific repeating DNA units of the domestic fowl, Gallus gallus domesticus. Chromosoma 96:18–25

    Article  CAS  PubMed  Google Scholar 

  • Lahn BT, Page DC (1999) Four evolutionary strata on the human X chromosome. Science 286:964

    Article  CAS  PubMed  Google Scholar 

  • Mank JE, Ellegren H (2007) Parallel divergence and degradation of the avian W sex chromosome. Trends Ecol Evol 22:389–391

    Article  PubMed  Google Scholar 

  • Matsubara K, Tarui H, Toriba M, Yamada K, Nishida-Umehara C, Agata K, Matsuda Y (2006) Evidence for different origin of sex chromosomes in snakes, birds, and mammals and step-wise differentiation of snake sex chromosomes. Proc Natl Acad Sci 103:18190

    Article  CAS  PubMed  Google Scholar 

  • Mengden GA (1981) Linear differentiation of the C-band pattern of the W chromosome in snakes and birds. Chromosoma 83:275–287

    Article  CAS  PubMed  Google Scholar 

  • Mengden GA (1982) Chromosomal evolution and the phylogeny of elapid snakes. PhD Thesis, Australian National University, Canberra

  • Mengden GA, Stock AD (1980) Chromosomal evolution in Serpentes; a comparison of G and C chromosome banding patterns of some colubrid and boid genera. Chromosoma 79:53–64

    Article  Google Scholar 

  • Muller HJ (1914) A gene for the fourth chromosome of Drosophila. J Exp Zool 17:325–336

    Article  Google Scholar 

  • Muller HJ (1918) Genetic variability, twin hybrids and constant hybrids, in a case of balanced lethal factors. Genetics 3:422–499

    CAS  PubMed  Google Scholar 

  • Nakatani Y, Takeda H, Kohara Y, Morishita S (2007) Reconstruction of the vertebrate ancestral genome reveals dynamic genome reorganization in early vertebrates. Genome Res 17:1254–1265

    Article  CAS  PubMed  Google Scholar 

  • Nanda I, Feichtinger W, Schmid M, Schröder JH, Zischler H, Epplen JT (1990) Simple repetitive sequences are associated with differentiation of the sex chromosomes in the guppy fish. J Mol Evol 30:456–462

    Article  CAS  Google Scholar 

  • Nanda I, Zischler H, Epplen C, Guttenbach M, Schmid M (1991) Chromosomal organization of simple repeated DNA sequences. Electrophoresis 12:193–203

    Article  CAS  PubMed  Google Scholar 

  • Nei M (1969) Linkage modification and sex difference in recombination. Genetics 63:681–699

    CAS  PubMed  Google Scholar 

  • Nicolas M et al (2005) A gradual process of recombination restriction in the evolutionary history of the sex chromosomes in dioecious plants. PLoS Biol 3:e4

    Article  PubMed  Google Scholar 

  • Ohno S (1967) Sex chromosomes and sex-linked genes. Springer, New York

    Google Scholar 

  • O’Meally D, Miller H, Patel H, Graves JAM, Ezaz T (2009) The first cytogenetic map of the tuatara, Sphenodon punctatus. Cytogenet Genome Res 127:213–223

    Article  PubMed  Google Scholar 

  • Parasnis AS, Ramakrishna W, Chowdari KV, Gupta VS, Ranjekar PK (1999) Microsatellite (GATA)n reveals sex-specific differences in Papaya. Theor Appl Genet 99:1047–1052

    Article  CAS  Google Scholar 

  • Parker J (1990) Sex-chromosome and sex differentiation in flowering plants. Chromosomes Today 10:187–198

    CAS  Google Scholar 

  • Porter CA, Hamilton MJ, Sites JW, Baker RJ (1991) Location of ribosomal DNA in chromosomes of squamate reptiles: systematic and evolutionary implications. Herpetologica 47:271–280

    Google Scholar 

  • Priyadarshini P, Murthy BS, Nagaraju J, Singh L (2003). A GATA-binding protein expressed predominantly in the pupal ovary of the silkworm, Bombyx mori. Insect Biochemistry and Molecular Biology 33:185–195

    Google Scholar 

  • Rice WR (1987) The accumulation of sexually antagonistic genes as a selective agent promoting the evolution of reduced recombination between primitive sex chromosomes. Evolution 41:911–914

    Article  Google Scholar 

  • Rice W (1996) Evolution of the Y sex chromosome in animals. Bioscience 46:331–343

    Article  Google Scholar 

  • Roger B, Moisand A, Amalric F, Bouvet P (2002) rDNA transcription during Xenopus laevis Oogenesis. Biochem Biophys Res Commun 290:1151–1160

    Article  CAS  PubMed  Google Scholar 

  • Saitoh Y, Mizuno S (1992) Distribution of XhoI and EcoRI family repetitive DNA sequences into separate domains in the chicken W chromosome. Chromosoma 101:474–477

    Article  CAS  PubMed  Google Scholar 

  • Sambrook J, Russell D (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory, Cold Spring Harbor

    Google Scholar 

  • Schäfer R, Böltz E, Becker A, Bartels F, Epplen JT (1986) The expression of the evolutionarily conserved GATA/GACA repeats in mouse tissues. Chromosoma 93:496–501

    Article  PubMed  Google Scholar 

  • Schoumans J, Nielsen K, Jeppesen I, Anderlid B, Blennow E, Brøndum-Nielsen K, Nordenskjöld M (2004) A comparison of different metaphase CGH methods for the detection of cryptic chromosome aberrations of defined size. Eur J Hum Genet: EJHG 12:447–454

    Article  CAS  PubMed  Google Scholar 

  • Shaw PJ, Jordan EG (1995) The nucleolus. Annu Rev Cell Dev Biol 11:93–121

    Article  CAS  PubMed  Google Scholar 

  • Shine R, Bull JJ (1977) Skewed sex ratios in snakes. Copeia 1977:228–234

    Article  Google Scholar 

  • Singh L, Purdom IF, Jones KW (1976) Satellite DNA and evolution of sex chromosomes. Chromosoma 59:43–62

    Article  CAS  PubMed  Google Scholar 

  • Singh L, Purdom IF, Jones KW (1981) Conserved Sex-chromosome-associated Nucleotide Sequences in Eukaryotes. Cold Spring Harb Symp Quant Biol 45:805–814

    CAS  PubMed  Google Scholar 

  • Skaletsky H et al (2003) The male-specific region of the human Y chromosome is a mosaic of discrete sequence classes. Nature 423:825–837

    Article  CAS  PubMed  Google Scholar 

  • Smit AFA, Hubley R, Green P (1996) RepeatMasker open-3.0. http://www.repeatmasker.org/

  • Smith JJ, Voss SR (2007) Bird and mammal sex-chromosome orthologs map to the same autosomal region in a salamander (Ambystoma). Genetics 177:607–613

    Article  CAS  PubMed  Google Scholar 

  • Solovei I, Ogawa A, Naito M, Mizuno S, Macgregor H (1998) Specific chromomeres on the chicken W lampbrush chromosome contain specific repetitive DNA sequence families. Chromosome Res 6:323–327

    Article  CAS  PubMed  Google Scholar 

  • Srikulnath K et al (2009) Karyotypic evolution in squamate reptiles: comparative gene mapping revealed highly conserved linkage homology between the butterfly lizard (Leiolepis reevesii rubritaeniata, Agamidae, Lacertilia) and the Japanese four-striped rat snake (Elaphe quadrivirgata, Colubridae, Serpentes). Chromosome Res 17:975–986

    Article  CAS  PubMed  Google Scholar 

  • Steinemann S, Steinemann M (2005) Retroelements: tools for sex chromosome evolution. Cytogenet Genome Res 110:134–143

    Article  CAS  PubMed  Google Scholar 

  • Stiglec R (2007) Comparative analysis of the chicken Z chromosome: implications for vertebrate sex chromosome evolution. PhD Thesis. Australian National University, Canberra

  • Suka N et al (1993) W-heterochromatin of chicken; its unusual DNA components, late replication, and chromatin structure. Genetica 88:93–105

    Article  CAS  PubMed  Google Scholar 

  • Telenius H et al (1992) Cytogenetic analysis by chromosome painting using DOP-PCR amplified flow-sorted chromosomes. Genes Chromosom Cancer 4:257–263

    Article  CAS  PubMed  Google Scholar 

  • Toder R, Wienberg J, Voullaire L, Maccarone P, Graves JAM (1997) Shared DNA sequences between the X and Y chromosomes in the tammar wallaby—evidence for independent additions to eutherian and marsupial sex chromosomes. Chromosoma 106:94–98

    Article  CAS  PubMed  Google Scholar 

  • Tone M, Sakaki Y, Hashiguchi T, Mizuno S (1984) Genus specificity and extensive methylation of the W chromosome-specific repetitive DNA sequences from the domestic fowl, Gallus gallus domesticus. Chromosoma 89:228–237

    Article  CAS  PubMed  Google Scholar 

  • Tsuda Y, Nishida-Umehara C, Ishijima J, Yamada K, Matsuda Y (2007) Comparison of the Z and W sex chromosomal architectures in elegant crested tinamou (Eudromia elegans) and ostrich (Struthio camelus) and the process of sex chromosome differentiation in palaeognathous birds. Chromosoma 116:159–173

    Article  PubMed  Google Scholar 

  • Vilella AJ et al (2009) EnsemblCompara genetrees: complete, duplication-aware phylogenetic trees in vertebrates. Genome Res 19:327–335

    Article  CAS  PubMed  Google Scholar 

  • Yamada K et al (2006) A novel family of repetitive DNA sequences amplified site-specifically on the W chromosomes in Neognathous birds. Chromosome Res 14:613–627

    Article  CAS  PubMed  Google Scholar 

  • Yoshido A et al (2007) FISH analysis of the W chromosome in Bombyx mandarina and several other species of lepidoptera by means of B. mori W-BAC probes. J Insect Biotechnol Sericology 76:1–7

    CAS  Google Scholar 

  • Vítková M et al (2007) Molecular divergence of the W chromosomes in pyralid moths (Lepidoptera). Chromosome Res 15:917–930

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

Animal collection, handling, sampling, and all other relevant procedures were performed following the guidelines of the Australian Capital Territory Animal Welfare Act 1992 (Section 40) under permits and licenses issued by Environment ACT, the New South Wales State, and Northern Territory governments (LI2008321, S12364, and 26791, respectively) and with the approval of the Australian National University Animal Experimentation Ethics Committee (Proposal R.CG.07.3b/04/07). We are grateful to John Cann, Paul Waters, and Beata Ujvari for providing specimens or assisting with collection and to two anonymous referees whose comments improved the paper substantially.

Author information

Authors and Affiliations

  1. Research School of Biology, Australian National University, Acton, ACT, 0200, Australia

    Denis O’Meally, Hardip R. Patel, Rami Stiglec, Jennifer A. Marshall Graves & Tariq Ezaz

  2. Institute for Applied Ecology, University of Canberra, Canberra, ACT, 2601, Australia

    Denis O’Meally, Stephen D. Sarre, Arthur Georges & Tariq Ezaz

Authors
  1. Denis O’Meally
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hardip R. Patel
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rami Stiglec
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Stephen D. Sarre
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Arthur Georges
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jennifer A. Marshall Graves
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Tariq Ezaz
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Denis O’Meally.

Additional information

Responsible Editor: Fengtang Yang.

Rights and permissions

Reprints and permissions

About this article

Cite this article

O’Meally, D., Patel, H.R., Stiglec, R. et al. Non-homologous sex chromosomes of birds and snakes share repetitive sequences. Chromosome Res 18, 787–800 (2010). https://doi.org/10.1007/s10577-010-9152-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10577-010-9152-9

Key words

Search

Navigation