Skip to main content
SpringerLink
Log in

Isolation and development of a molecular sex marker for Bassiana duperreyi, a lizard with XX/XY sex chromosomes and temperature-induced sex reversal

  • Original Paper
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

Sex determination in the endemic Australian lizard Bassiana duperreyi (Scincidae) is influenced by sex chromosomes and incubation temperature, challenging the traditional dichotomy in reptilian sex determination. Analysis of those interactions requires sex chromosome markers to identify temperature-induced sex reversal. Here, we report the isolation of Y chromosome DNA sequence from B. duperreyi using amplified fragment length polymorphism PCR, the conversion of that sequence to a single-locus assay, and its combination with a single-copy nuclear gene (C-mos) to form a duplex PCR test for chromosomal sex. The accuracy of the assay was tested on an independent panel of individuals with known phenotypic sex. When used on offspring from field nests, our test identified the likely occurrence of a low rate of natural sex reversal in this species. This work represents the first report of Y chromosome sequence from a reptile and one of the few reptile sex tests.

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

Similar content being viewed by others

References

  • Bull JJ (1980) Sex determination in reptiles. Q Rev Biol 55:3–21

    Article  Google Scholar 

  • Bull JJ, Vogt RC (1979) Temperature-dependent sex determination in turtles. Science 206:186–1188

    Article  Google Scholar 

  • Burger J, Zappalorti RT (1988) Effects of incubation temperatures on sex ratios in pine snakes: differential vulnerability of males and females. Am Nat 132:492–505

    Article  Google Scholar 

  • Conover DO (2004) Temperature-dependent sex determination in fishes. In: Valuenzuela N, Lance VA (eds) Temperature-dependent sex determination in vertebrates. Smithsonian Institute, Washington, pp 11–20

    Google Scholar 

  • Conover DO, Kynard BE (1981) Environmental sex determination: interaction of temperature and genotype in a fish. Science 213:577–579

    Article  PubMed  Google Scholar 

  • Cooper SJB, Bull CM, Gardner MG (1997) Characterisation of microsatellite loci from the social monogamous lizard Tiliqua rugosa using a PCR-based isolation technique. Mol Ecol 6:793–795

    Article  PubMed  CAS  Google Scholar 

  • Devlin RH, Nagahama Y (2002) Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture 208:191–364

    Article  CAS  Google Scholar 

  • Donnellan SC (1985) The evolution of sex chromosomes in scincid lizards. PhD thesis. Macquarie University, Sydney

    Google Scholar 

  • Donnellan SC (1991) Chromosomes of Australian lygosomine skinks (Lacertilia, Scincidae) II. The genus Lampropholis. Genetica 83:223–234

    Article  Google Scholar 

  • Ezaz T, Harvey SC et al (2004) Isolation and physical mapping of sex-linked AFLP markers in Nile tilapia (Oreochromis niloticus L.). Mar Biotech 6:435–445

    Article  CAS  Google Scholar 

  • Ezaz T, Stiglec R, Veyrunes F, Graves JAM (2006) Relationships between vertebrate ZW and XY sex chromosome systems. Curr Biol 16:736–743

    Article  Google Scholar 

  • Felip A, Young WP et al (2005) An AFLP-based approach for the identification of sex-linked markers in rainbow trout (Oncorhynchus mykiss). Aquaculture 247:35–43

    Article  CAS  Google Scholar 

  • Graves JAM (2006) Sex chromosome specialization and degeneration in mammals. Cell 124:901–912

    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 290:449–462

    Article  Google Scholar 

  • Griffiths R (2000) Sex identification using DNA markers. In: Baker AJ (ed) Molecular methods in ecology. Blackwell, London, pp 295–322

    Google Scholar 

  • Griffiths R, Orr KJ (1999) The use of amplified fragment length polymorphism (AFLP) in the isolation of sex-specific markers. Mol Ecol 8:671–674

    Article  PubMed  CAS  Google Scholar 

  • Griffiths R, Orr KJ, Adam A, Barber I (2000) DNA sex identification in the three-spined stickleback. J Fish Biol 57:1331–1334

    Article  CAS  Google Scholar 

  • Halverson J, Spelman LH (2002) Sex determination. In: Murphy JB, Ciofi C, de la Panouse C, Walsh T (eds) Biology and conservation of Komodo dragons. Smithsonian Institute, Washington, pp 165–177

    Google Scholar 

  • Hardy GM (1979) The karyotypes of two scincid lizards, and their bearing on relationships in genus Leiolopisma and relatives (Scincidae: Lygosominae). N Z J Zool 6:609–612

    Google Scholar 

  • Harlow PS (1996) A harmless technique for sexing hatchling lizards. Herp Rev 27:71–72

    Google Scholar 

  • Hutchinson MN, Donnellan SC (1992) Taxonomy and geographic variation in the Australian lizards of the genus Pseudemoia (Scincidae: Lygosominae). J Nat Hist 26:215–264

    Article  Google Scholar 

  • Janzen FJ, Paukstis GL (1991) Environmental sex determination in reptiles: ecology, evolution, and experimental design. Q Rev Biol 66:149–179

    Article  PubMed  CAS  Google Scholar 

  • Lebel-Hardenack S, Hauser E, Law TF, Schmid J, Grant SR (2002) Mapping of sex determination loci on the white campion (Silene latifolia) Y chromosome using amplified fragment length polymorphism. Genetics 160:717–725

    PubMed  CAS  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 USA 103:18190–18195

    Article  PubMed  CAS  Google Scholar 

  • Miller SA, Dykes DD, Polesky HF (1988) A simple salting-out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res 16:1215

    Article  PubMed  CAS  Google Scholar 

  • Nanda I, Zend-Ajusch E et al (2000) Conserved synteny between the chicken Z sex chromosome and human chromosome 9 includes the male regulatory gene DMRT1: a comparative (re)view on avian sex determination. Cytogenet Cell Genet 89:67–78

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Olmo E (1986) Animal cytogenetics 4, chordata 3, A. reptilia. Gebruder Borntraeger, Stuttgart

    Google Scholar 

  • Peil A, Flachowsky H, Schumann E, Weber WE (2003) Sex-linked AFLP markers indicate a pseudoautosomal region in hemp (Cannabis sativa L.). Theor Appl Genet 107:102–109

    PubMed  CAS  Google Scholar 

  • Quinn AE, Georges A, Sarre SD, Guarino F, Ezaz T, Graves JAM (2007) Temperature sex reversal implies sex gene dosage in a reptile. Science 316:411

    Article  PubMed  CAS  Google Scholar 

  • Radder RS, Ali S, Shine R (2007) Offspring sex is not related to maternal allocation of yolk steroids in the lizard Bassiana duperreyi (Scincidae). Physiol Biochem Zool 80:220–227

    Article  PubMed  CAS  Google Scholar 

  • Radder RS, Quinn AE, Georges A, Sarre SD, Shine R (2008) Genetic evidence for co-occurrence of chromosomal and thermal sex-determining systems in a lizard. Biol Lett 4:176–178

    Article  PubMed  CAS  Google Scholar 

  • Reamon-Büttner SM, Schondelmaier J, Jung C (1998) AFLP markers tightly linked to the sex locus in Asparagus officinalis L. Mol Breed 4:91–98

    Article  Google Scholar 

  • Saint KM, Austin CC, Donnellan SC, Hutchinson MN (1998) C-mos, a nuclear marker useful for squamate phylogenetic analysis. Mol Phylogenet Evol 10:259–263

    Article  PubMed  CAS  Google Scholar 

  • Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, New York

    Google Scholar 

  • Sarre SD, Georges A, Quinn AE (2004) The ends of a continuum: genetic and temperature-dependent sex determination in reptiles. BioEssays 26:639–645

    Article  PubMed  Google Scholar 

  • Shine R, Elphick MJ, Donnellan SC (2002) Co-occurrence of multiple, supposedly incompatible modes of sex determination in a lizard population. Ecol Lett 5:486–489

    Article  Google Scholar 

  • Solari AJ (1994) Sex chromosomes and sex determination in vertebrates. CRC, Boca Raton

    Google Scholar 

  • Stiglec R, Ezaz T, Graves JAM (2007) A new look at the evolution of avian sex chromosomes. Cytogenet Genome Res 117:103–109

    Article  PubMed  CAS  Google Scholar 

  • Stow AJ, Sunnucks P, Briscoe DA, Gardner MG (2001) The impact of habitat fragmentation on dispersal of Cunningham’s skink (Egernia cunninghami): evidence from allelic and genotypic analyses of microsatellites. Mol Ecol 10:867–878

    Article  PubMed  CAS  Google Scholar 

  • Valenzuela N, Lance VA (eds) (2004) Temperature-dependent sex determination in vertebrates. Smithsonian Institute, Washington

    Google Scholar 

  • Valenzuela N, Adams DC, Janzen FJ (2003) Pattern does not equal process: exactly when is sex environmentally determined? Am Nat 161:676–683

    Article  PubMed  Google Scholar 

  • Vos P, Hogers R, Bleeker M, Reijans M, van de Lee T, Homes M, Frijters A, Pot J, Peleman J, Kuiper M, Zabeau M (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 23:4407–4414

    Article  PubMed  CAS  Google Scholar 

  • Welsh J, McClelland M (1990) Fingerprinting genomes using PCR with arbitrary primers. Nucleic Acids Res 18:7213–7218

    Article  PubMed  CAS  Google Scholar 

  • Williams JGK, Kubelik AR, Livak KJ, Rafalski JA, Tingey SV (1990) DNA polymorphisms amplified by arbitrary primers are useful as genetic markers. Nucleic Acids Res 18:6531–6535

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Melanie Elphick and Jacqui Richardson for laboratory assistance, and the Australian Research Council (DP0346850 to SDS and AG, DP0449935 to JM Graves, SDS and AG, and FF561365 to RS) for funding. We are deeply indebted to our late colleague Raju Radder who died unexpectedly at the age of 34 before this manuscript was finalized.

Author information

Authors and Affiliations

  1. Institute for Applied Ecology, University of Canberra, Canberra, Australia

    Alexander E. Quinn, Stephen D. Sarre, Arthur Georges & Tariq Ezaz

  2. School of Biological Sciences A08, University of Sydney, Sydney, Australia

    Rajkumar S. Radder & Richard Shine

  3. Comparative Genomics Group, Research School of Biological Sciences, Australian National University, Canberra, Australia

    Tariq Ezaz

Authors
  1. Alexander E. Quinn
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rajkumar S. Radder
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Stephen D. Sarre
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Arthur Georges
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Tariq Ezaz
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Richard Shine
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Stephen D. Sarre.

Additional information

Communicated by T. Becker.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Quinn, A.E., Radder, R.S., Sarre, S.D. et al. Isolation and development of a molecular sex marker for Bassiana duperreyi, a lizard with XX/XY sex chromosomes and temperature-induced sex reversal. Mol Genet Genomics 281, 665–672 (2009). https://doi.org/10.1007/s00438-009-0437-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-009-0437-7

Keywords

Search

Navigation