Skip to main content
SpringerLink
Log in

An XX/XY heteromorphic sex chromosome system in the Australian chelid turtle Emydura macquarii: A new piece in the puzzle of sex chromosome evolution in turtles

  • Published:
Chromosome Research Aims and scope Submit manuscript

Abstract

Chromosomal sex determination is the prevalent system found in animals but is rare among turtles. In fact, heteromorphic sex chromosomes are known in only seven of the turtles possessing genotypic sex determination (GSD), two of which correspond to cryptic sex microchromosomes detectable only with high-resolution cytogenetic techniques. Sex chromosomes were undetected in previous studies of Emydura macquarii, a GSD side-necked turtle. Using comparative genomic hybridization (CGH) and GTG-banding, a heteromorphic XX/XY sex chromosome system was detected in E. macquarii. The Y chromosome appears submetacentric and somewhat larger than the metacentric X, the first such report for turtles. CGH revealed a male-specific chromosomal region, which appeared heteromorphic using GTG-banding, and was restricted to the telomeric region of the p arm. Based on our observations and the current phylogeny of chelid turtles, we hypothesize that the sex chromosomes of E. macquarii might be the result of a translocation of an ancestral Y microchromosome as found in a turtle belonging to a sister clade, Chelodina longicollis, onto the tip of an autosome. However, in the absence of data from an outgroup, the opposite (fission of a large XY into an autosome and a micro-XY) is theoretically equally likely. Alternatively, the sex chromosome systems of E. macquarii and C. longicollis may have evolved independently. We discuss the potential causes and consequences of such putative chromosome rearrangements in the evolution of sex chromosomes and sex-determining systems of turtles in general.

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

  • Almeida-Toledo LF, Foresti F, Daniel MFZ, Toledo SA (2000) Sex chromosome evolution in fish: the formation of the neo-Y chromosome in Eigenmannia (Gymnotiformes). Chromosoma 109: 197–200.

    Article  PubMed  CAS  Google Scholar 

  • Ayala FJ, Coluzzi M (2005) Chromosome speciation: Humans, Drosophila, and mosquitoes. Proc Natl Acad Sci U S A 102: 6535–6542.

    Article  PubMed  CAS  Google Scholar 

  • Ayres M, Sampaio MM, Barros RMS, Dias LB, Cunha OR (1969) A karyological study of turtles from the Brazilian Amazon Region. Cytogenetics 8: 401–409.

    Article  PubMed  CAS  Google Scholar 

  • Barros RM, Sampaio MM, Assis MF, Ayres M, Cunha OR (1976) General considerations on the Karyotypic Evolution of Chelonia from the Amazon Region of Brazil. Cytologia 41: 559–565.

    Google Scholar 

  • Berry JF, Shine R (1980) Sexual size dimorphism and sexual selection in turtles (Order Testudines). Oecologia 44: 185–191.

    Article  Google Scholar 

  • Bull JJ (1983) Evolution of Sex Determining Mechanisms. Menlo Park, CA: Benjamin/Cummings.

    Google Scholar 

  • Bull JJ, Legler JM (1980) Karyotypes of side-necked turtles (Testudines: Pleurodira). Can J Zool 58: 828–841.

    Article  Google Scholar 

  • Bull JJ, Moon RG, Legler JM (1974) Male heterogamety in kinosternid turtles (genus Staurotypus). Cytogenet Cell Genet 13: 419–425.

    Article  PubMed  CAS  Google Scholar 

  • Carr JL, Bickham JW (1981) Sex-chromosomes of the Asian black pond turtle, Siebenrockiella crassicollis (Testudines, Emydidae). Cytogenet Cell Genet 31: 178–183.

    Article  PubMed  CAS  Google Scholar 

  • Carvalho AB, Clark AG (2005) Y chromosome of D-pseudoobscura is not homologous to the ancestral Drosophila Y. Science 307: 108–110.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Charlesworth B, Coyne JA, Barton NH (1987) The relative rates of evolution of sex chromosomes and autosomes. Am Nat 130: 113–146.

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Coghlan A, Eichler EE, Oliver SG, Paterson AH, Stein L (2005) Chromosome evolution in eukaryotes: a multi-kingdom perspective. Trends Genet 21: 673–682.

    Article  PubMed  CAS  Google Scholar 

  • Edwards SV, Kingan SB, Calkins JD et al. (2005) Speciation in birds: Genes, geography, and sexual selection. Proc Natl Acad Sci U S A 102: 6550–6557.

    Article  PubMed  CAS  Google Scholar 

  • Ezaz MT, McAndrew BJ, Penman DJ (2004) Spontaneous diploidization of the maternal chromosome set in Nile tilapia (Oreochromis niloticus L.) eggs. Aquaculture Res 35: 271–277.

    Article  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  PubMed  CAS  Google Scholar 

  • Ezaz T, Valenzuela N, Grutzner F et al. (2006) An XX/XY sex microchromosome system in a freshwater turtle, Chelodina longicollis (Testudines: Chelidae) with genetic sex determination. Chromosome Res 14: 139–150.

    Article  PubMed  CAS  Google Scholar 

  • Georges A, Thomson S (2006) Evolution and zoogeography of Australian freshwater turtles. In: Merrick JR, Archer M, Hickey G, Lee M, eds. Evolution and Zoogeography of Australasian Vertebrates. Sydney: Australia: AUSCIPUB (Australian Scientific Publishing) Pty Ltd.

    Google Scholar 

  • Graves JAM (2002) The rise and fall of SRY. Trends Genet 18: 259–264.

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Grutzner F, Rens W, Tsend-Ayush E et al. (2004) In the platypus a meiotic chain of ten sex chromosomes shares genes with the bird Z and mammal X chromosomes. Nature 432: 913–917.

    Article  PubMed  CAS  Google Scholar 

  • Iverson JB, Brown RM, Akre TS et al. (2007) In search of the tree of life for turtles. Chelonian Res Monogr 4: 85–106.

    Google Scholar 

  • Just W, Baumstark A, Sub A et al. (2007) Ellobius lutescens: sex determination and sex chromosome. Sex Dev 1: 211–221.

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Killebrew F (1976) Mitotic chromosomes of turtles. II. The Chelidae. Texas J Sci 27: 149–154.

    Google Scholar 

  • Lewis KR, John B (1963) Chromosome Marker. Boston : Little Brown.

    Google Scholar 

  • Lindholm A, Breden F (2002) Sex chromosomes and sexual selection in poeciliid fishes. Am Nat 160: S214–S224.

    Article  PubMed  Google Scholar 

  • Liu ZY, Moore PH, Ma H et al. (2004) A primitive Y chromosome in papaya marks incipient sex chromosome evolution. Nature 427: 348–352.

    Article  PubMed  CAS  Google Scholar 

  • Masly JP, Jones CD, Noor MAF, Locke J, Orr HA (2006) Gene transposition as a cause of hybrid sterility in Drosophila. Science 313: 1448–1450.

    Article  PubMed  CAS  Google Scholar 

  • Matsunaga S, Kawano S (2001) Sex determination by sex chromosomes in dioecious plants. Plant Biol 3: 481–488.

    Article  Google Scholar 

  • McBee K, Bickham JW, Rhodin AGJ, Mittermeier RA (1985) Karyotypic variation in the genus Platemys (Testudines, Pleurodira). Copeia 2: 445–449.

    Article  Google Scholar 

  • Ming R, Yu QY, Moore PH (2007) Sex determination in papaya. Semin Cell DevBiol 18: 401–408.

    Article  CAS  Google Scholar 

  • Modi WS, Crews D (2005) Sex chromosomes and sex determination in reptiles—Commentary. Curr Opin Genet Dev 15: 660–665.

    Article  PubMed  CAS  Google Scholar 

  • Near TJ, Meylan PA, Shaffer HB (2005) Assessing concordance of fossil calibration points in molecular clock studies: an example using turtles. Am Nat 165: 137–146.

    Article  PubMed  Google Scholar 

  • Ohno S (1967) Sex Chromosomes and Sex-linked Genes. Berlin: Springer.

    Google Scholar 

  • Peichel CL, Ross JA, Matson CK et al. (2004) The master sex-determination locus in Threespine Sticklebacks is on a nascent Y chromosome. Curr Biol 14: 1416–1424.

    Article  PubMed  CAS  Google Scholar 

  • Rhodin AGJ, Mittermeier RA, Gardner AL, Medem F (1978) Karyotypic analysis of the Podocnemis turtles. Copeia 4: 723–728.

    Article  Google Scholar 

  • Rhodin AGJ, Mittermeier RA, McMorris JR (1984) Platemys Macrocephala, a new species of Chelid turtle from Central Bolivia and the Pantanal Region of Brazil. Herpetologica 40: 38–46.

    Google Scholar 

  • Rice WR (1984) Sex-chromosomes and the evolution of sexual dimorphism. Evolution 38: 735–742.

    Article  Google Scholar 

  • Sato M, Ikeda M (1992) Chromosomal complements of 2 forms of Neanthes japonica (Polychaeta, Nereeididae) with evidence of male-heterogametic sex-chromosomes. Mar Biol 112:299–307.

    Article  Google Scholar 

  • Saether SA, Saetre GP, Borge T et al. (2007) Sex chromosome-linked species recognition and evolution of reproductive isolation in flycatchers. Science 318: 95–97.

    Article  PubMed  CAS  Google Scholar 

  • Schmid M, Steinlein C (1991) Chromosome-banding in Amphibia .16. High-resolution replication banding-patterns in Xenopus laevis. Chromosoma 101: 123–132.

    Article  PubMed  CAS  Google Scholar 

  • Sharma GP, Kaur P, Nakhasi U (1975) Female heterogamety in the Indian crytodiran Chelonian, Kachuga Smithi Gray. In Tiwari KK, Srivistava CB, eds. Dr. B.S. Chauhan Commemoration Volume 359–368. Zoological Society of India, Orissa.

  • Sites JWJ, Bickham JW, Haiduk MW, Iverson JB (1979) Banded karyotypes of six taxa of kinosternid turtles. Copeia 4: 692–698.

    Article  Google Scholar 

  • Solari AJ (1994) Sex Chromosomes and Sex Determination in Vertebrates. Boca Raton, FL: CRC Press.

    Google Scholar 

  • Thompson MB (1988) Influence of incubation temperature and water potential on sex determination in Emydura macquarii (Testudines: Pleurodira). Herpetologica 44: 86–90.

    Google Scholar 

  • Valenzuela N (2004) Temperature-dependent sex determination. In: Deeming DC, ed. Reptilian Incubation: Environment & Behaviour. Nottingham, UK: Nottingham University Press, pp. 211–227.

    Google Scholar 

  • Valenzuela N, Lance VA, eds. (2004) Temperature Dependent Sex Determination in Vertebrates. Washington, DC: Smithsonian Books.

    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 

  • Vallender EJ, Lahn BT (2004) How mammalian sex chromosomes acquired their peculiar gene content. Bioessays 26: 159–169.

    Article  PubMed  CAS  Google Scholar 

  • Van Doorn GS, Kirkpatrick M (2007) Turnover of sex chromosomes induced by sexual conflict. Nature 449: 909–912.

    Article  PubMed  CAS  Google Scholar 

  • Waters PD, Wallis MC, Graves JAM (2007) Mammalian sex—Origin and evolution of the Y chromosome and SRY. Semin Cell Dev Biol 18: 389–400.

    Article  PubMed  CAS  Google Scholar 

  • White MJD (1968) Models of speciation. Science 159: 1065–1070.

    Article  PubMed  CAS  Google Scholar 

  • White MJD (1973) Animal Cytology and Evolution, 3rd edn. Cambridge: Cambridge University Press.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Ecology, Evolution, and Organismal Biology, Iowa State University, 253 Bessey Hall, Ames, IA, 50011, USA

    Pedro Alonzo Martinez & Nicole Valenzuela

  2. Comparative Genomics Group, Research School of Biological Sciences, The Australian National University, Canberra, ACT, 2601, Australia

    Tariq Ezaz & Jennifer A. Marshall Graves

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

    Arthur Georges

Authors
  1. Pedro Alonzo Martinez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tariq Ezaz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nicole Valenzuela
    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. Jennifer A. Marshall Graves
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Pedro Alonzo Martinez.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Martinez, P.A., Ezaz, T., Valenzuela, N. et al. An XX/XY heteromorphic sex chromosome system in the Australian chelid turtle Emydura macquarii: A new piece in the puzzle of sex chromosome evolution in turtles. Chromosome Res 16, 815–825 (2008). https://doi.org/10.1007/s10577-008-1228-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10577-008-1228-4

Key words

Search

Navigation