Chromosome Research

, Volume 18, Issue 7, pp 787–800 | Cite as

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

  • Denis O’Meally
  • Hardip R. Patel
  • Rami Stiglec
  • Stephen D. Sarre
  • Arthur Georges
  • Jennifer A. Marshall Graves
  • Tariq Ezaz
Article

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.

Key words

Aves Bkm degeneration evolution Serpentes sex chromosomes repeats 

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

Notes

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.

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Copyright information

© Springer Science + Business Media B.V. 2010

Authors and Affiliations

  • Denis O’Meally
    • 1
    • 2
  • Hardip R. Patel
    • 1
  • Rami Stiglec
    • 1
  • Stephen D. Sarre
    • 2
  • Arthur Georges
    • 2
  • Jennifer A. Marshall Graves
    • 1
  • Tariq Ezaz
    • 1
    • 2
  1. 1.Research School of BiologyAustralian National UniversityActonAustralia
  2. 2.Institute for Applied EcologyUniversity of CanberraCanberraAustralia

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