Karyotypic analysis and FISH mapping of microsatellite motifs reveal highly differentiated XX/XY sex chromosomes in the pink-tailed worm-lizard (Aprasia parapulchella, Pygopodidae, Squamata)

Molecular Cytogenetics

Tariq Ezaz¹  Arthur Georges¹  Stephen D Sarre¹  Theresa Knopp¹  Kazumi Matsubara¹ 

[1] Institute for Applied Ecology, University of Canberra, Canberra ACT 2601, Australia

关键词: Y chromosome degeneration;    Sex chromosome differentiation;    Reptile;   

Others  :  1150520
DOI  :  10.1186/1755-8166-6-60

 received in 2013-10-19, accepted in 2013-11-23,  发布年份 2013

【 摘 要 】

Background

The infraorder Gekkota is intriguing because it contains multiple chromosomal and environmental sex determination systems that vary even among closely related taxa. Here, we compare male and females karyotypes of the pink-tailed worm-lizard (Aprasia parapulchella), a small legless lizard belonging to the endemic Australian family Pygopodidae.

Results

We applied comparative genomic hybridization to reveal an XX/XY sex chromosome system in which the Y chromosome is highly differentiated from the X in both gross morphology and DNA sequence. In addition, FISH mapping has revealed that two microsatellite repeat motifs, (AGAT)n and (AC)n, have been amplified multiple times on the Y chromosome.

Conclusion

XY karyotypes are found in other pygopodids (Delma inornata and Lialis burtonis), suggesting that the common ancestor of Pygopodidae also had XY sex chromosomes. However, the morphology and size of the Y chromosomes are different among the three species, suggesting that the processes underlying the evolution of sex chromosomes in the Pygopodidae involved chromosome rearrangements and accumulation and amplification of repeats.

【 授权许可】

   
2013 Matsubara et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

【 参考文献 】

• [1]Ezaz T, Stiglec R, Veyrunes F, Graves JAM: Relationships between vertebrate ZW and XY sex chromosome systems. Curr Biol 2006, 16:R736-R743.
• [2]Ezaz T, Sarre SD, O’Meally , Graves JAM, Georges A: Sex chromosome evolution in lizards: independent origins and rapid transitions. Cytogenet Genome Res 2009, 127:249-260.
• [3]Quinn AE, Georges A, Sarre SD, Guarino F, Ezaz T, Graves JA: Temperature sex reversal implies sex gene dosage in a reptile. Science 2007, 316:411.
• [4]Radder RS, Quinn AE, Georges A, Sarre SD, Shine R: Genetic evidence for co-occurrence of chromosomal and thermal sex-determining systems in a lizard. Biol Lett 2008, 4:176-178.
• [5]Sarre SD, Ezaz T, Georges A: Transitions between sex-determining systems in reptiles and amphibians. Annu Rev Genomics Hum Genet 2011, 12:391-406.
• [6]Vidal N, Hedges SB: Lizards, snakes, and amphisbaenians (Squamata). In The Timetree of Life. Edited by Hedges SB, Kumar S. New York: Oxford University Press; 2009:383-389.
• [7]Gamble T: A review of sex determining mechanisms in geckos (Gekkota: Squamata). Sex Dev 2010, 4:88-103.
• [8]Jennings WB, Pianka ER, Donnellan S: Systematics of the lizard family pygopodidae with implications for the diversification of Australian temperate biotas. Syst Biol 2003, 52:757-780.
• [9]Oliver PM, Sanders KL: Molecular evidence for Gondwanan origins of multiple lineages within a diverse Australasian gecko radiation. J Biogeogr 2009, 36:2044-2055.
• [10]Kluge AG: A taxonomic revision of the lizard family Pygopodidae. Miscellaneous Publications Museum of Zoology, University of Michigan 1974, 147:1-221.
• [11]Wilson S, Swan G: A complete guide to reptiles Australia. 3rd edition. Chatswood, Australia: New Holland Publisher Australia; 2010.
• [12]Olmo E, Signorino GG: Chromorep: A reptile chromosomes database. [http://chromorep.univpm.it/ webcite]
• [13]Gorman GC, Gress F: Sex chromosomes of a pygopodid lizard, Lialis burtonis. Experientia 1970, 26:206-207.
• [14]King M: Chromosomal and immunogenetic data: A new perspective on the origin of Australia’s reptiles. In Cytogenetics of Amphibians and Reptiles. Edited by Olmo E. Basel: Birkhäuser; 1990:153-180.
• [15]Kluge AG: Phylogenetic relationships in the lizard family pygopodidae: an evaluation of theory, methods and data. Miscellaneous Publications Museum of Zoology, University of Michigan 1976, 152:1-72.
• [16]Knopp T, Sarre SD: Identification of microsatellite markers for the pink-tailed worm-lizard, Aprasia parapulchella (kluge): an endangered pygopodid. Conservation Genetics and Resource 2012, 4:733-735.
• [17]King M: Chromosomal evolution in the Diplodactylinae (gekkonidae: reptilia). I. Evolutionary relationships and patterns of change. Aust J Zool 1987, 35:507-531.
• [18]Rice WR: The accumulation of sexually antagonistic genes as a selective agent promoting the evolution of reduced recombination between primitive sex chromosomes. Evolution 1987, 41:911-914.
• [19]Charlesworth B, Charlesworth D: The degeneration of Y chromosomes. Philos Trans R Soc Lond B Biol Sci 2000, 355:1563-1572.
• [20]Charlesworth D, Charlesworth B, Marais G: Steps in the evolution of heteromorphic sex chromosomes. Heredity 2005, 95:118-128.
• [21]Nanda I, Feichtinger W, Schmid M, Schröder JH, Zischler H, Epplen JT: Simple repetitive sequences are associated with differentiation of the sex chromosomes in the guppy fish. J Mol Evo 1990, 30:456-462.
• [22]Kraemer C, Schmidt ER: The sex determining region of Chironomus thummi is associated with highly repetitive DNA and transposable elements. Chromosoma 1993, 102:553-562.
• [23]Erlandsson R, Wilson JF, Pääbo S: Sex chromosomal transposable element accumulation and male-driven substitutional evolution in humans. Mol Biol Evol 2000, 17:804-812.
• [24]Harvey SC, Boonphakdee C, Campos-Ramos R, Ezaz MT, Griffin DK, Bromage NR Penman DJ: Analysis of repetitive DNA sequences in the sex chromosomes of Oreochromis niloticus. Cytogenet Genome Res 2003, 101:314-319.
• [25]Liu Z, Moore PH, Ma H, Ackerman CM, Ragiba M, Yu Q, Pearl HM, Kim MS, Charlton JW, Stiles JI, Zee FT, Paterson AH, Ming R: A primitive Y chromosome in papaya marks incipient sex chromosome evolution. Nature 2004, 427:348-352.
• [26]Hobza R, Lengerova M, Svoboda J, Kubekova H, Kejnovsky E, Vyskot B: An accumulation of tandem DNA repeats on the Y chromosome in Silene latifolia during early stages of sex chromosome evolution. Chromosoma 2006, 115:376-382.
• [27]Kawai A, Nishida-Umehara C, Ishijima J, Tsuda Y, Ota H, Matsuda Y: Different origins of bird and reptile sex chromosomes inferred from comparative mapping of chicken Z-linked genes. Cytogenet Genome Res 2007, 117:92-102.
• [28]O’Meally D, Patel HR, Stiglec R, Sarre SD, Georges A, Graves JAM, Ezaz T: Non-homologous sex chromosomes of birds and snakes share repetitive sequences. Chromosome Res 2010, 18:787-800.
• [29]Cioffi MB, Camacho JPM, Bertollo LAC: Repetitive DNAs and differentiation of sex chromosomes in neotropical fishes. Cytogenet Genome Res 2011, 132:188-194.
• [30]Pokorná M, Kratochvíl L, Kejnovský E: Microsatellite distribution on sex chromosomes at different stages of heteromorphism and heterochromatinization in two lizard species (Squamata: Eublepharidae: Coleonyx elegans and Lacertidae: Eremias velox). BMC Genet 2011, 12:90. BioMed Central Full Text
• [31]Ezaz T, O’Meally D, Quinn AE, Sarre SD, Georges A, Graves JAM: A simple non-invasive protocol to establish primary cell lines from tail and toe explants for cytogenetic studies in Australian dragon lizards (Squamata: Agamidae). Cytotechnology 2008, 58:135-139.
• [32]Ezaz T, Quinn AE, Miura I, Sarre SD, Georges A, Graves JAM: The dragon lizard Pogona vitticeps has ZZ/ZW micro-sex chromosomes. Chromosome Res 2005, 13:763-776.