Discovery of the youngest sex chromosomes reveals first case of convergent co-option of ancestral autosomes in turtles
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Most turtle species possess temperature-dependent sex determination (TSD), but genotypic sex determination (GSD) has evolved multiple times independently from the TSD ancestral condition. GSD in animals typically involves sex chromosomes, yet the sex chromosome system of only 9 out of 18 known GSD turtles has been characterized. Here, we combine comparative genome hybridization (CGH) and BAC clone fluorescent in situ hybridization (BAC FISH) to identify a macro-chromosome XX/XY system in the GSD wood turtle Glyptemys insculpta (GIN), the youngest known sex chromosomes in chelonians (8–20 My old). Comparative analyses show that GIN-X/Y is homologous to chromosome 4 of Chrysemys picta (CPI) painted turtles, chromosome 5 of Gallus gallus chicken, and thus to the X/Y sex chromosomes of Siebenrockiella crassicollis black marsh turtles. We tentatively assign the gene content of the mapped BACs from CPI chromosome 4 (CPI-4) to GIN-X/Y. Chromosomal rearrangements were detected in G. insculpta sex chromosome pair that co-localize with the male-specific region of GIN-Y and encompass a gene involved in sexual development (Wt1—a putative master gene in TSD turtles). Such inversions may have mediated the divergence of G. insculpta sex chromosome pair and facilitated GSD evolution in this turtle. Our results illuminate the structure, origin, and evolution of sex chromosomes in G. insculpta and reveal the first case of convergent co-option of an autosomal pair as sex chromosomes within chelonians.
KeywordsEvolution of genome and sex chromosome organization Genotypic and temperature-dependent sex determination Comparative genome and BAC in situ hybridization molecular cytogenetics Turtle reptile vertebrates Convergent ancestral reconstruction Wt1 chromosomal rearrangement
We thank Steve DeSimone (director of the Cold Spring Harbor Fish Hatchery and Aquarium) for the access to specimens for sampling and R. Literman for the help with DNA extractions. This work was funded in part by NSF grant MCB 1244355 to NV.
Compliance with ethical standards
All procedures were approved by the IACUC of Iowa State University and were carried out under appropriate local permits. This article does not contain any studies with human participants.
Conflict of interest
The authors declare that they have no competing interests.
- Badenhorst D, Hillier LW, Literman R, Montiel EE, Radhakrishnan S, Shen Y, Minx P, Janes DE, Warren WC, Edwards SV, Valenzuela N (2015) Physical mapping and refinement of the painted turtle genome (Chrysemys picta) inform amniote genome evolution and challenge turtle-bird chromosomal conservation. Genome Biol Evol 7:2038–2050CrossRefPubMedPubMedCentralGoogle Scholar
- Bickham JW (1975) A cytosystematic study of turtles in the genera Clemmys, Mauremys and Sacalia. Herpetologica 31:198–204Google Scholar
- Chen S, Zhang G, Shao C, Huang Q, Liu G, Zhang P, Song W, An N, Chalopin D, Volff J-N, Hong Y, Li Q, Sha Z, Zhou H, Xie M, Yu Q, Liu Y, Xiang H, Wang N, Wu K, Yang C, Zhou Q, Liao X, Yang L, Hu Q, Zhang J, Meng L, Jin L, Tian Y, Lian J, Yang J, Miao G, Liu S, Liang Z, Yan F, Li Y, Sun B, Zhang H, Zhang J, Zhu Y, Du M, Zhao Y, Schartl M, Tang Q, Wang J (2014) Whole-genome sequence of a flatfish provides insights into ZW sex chromosome evolution and adaptation to a benthic lifestyle. Nat Genet 46:253−+CrossRefPubMedGoogle Scholar
- Devlin RH, Stone GW, Smailus DE (1998) Extensive direct-tandem organization of a long repeat DNA sequence on the Y chromosome of Chinook salmon (Oncorhynchus tshawytscha). J Mol Evol 46:277–287Google Scholar
- Ernst CH, Lovich JE (2009) Turtles of the United States and Canada. JHU PressGoogle Scholar
- Ewert MA, Etchberger CR, Nelson CE (2004) Turtle sex determining modes and TSD patterns, and some TSD pattern correlates. In: Valenzuela N, Lance VA (eds) Temperature dependent sex determination in vertebrates. Smithsonian Books, Washington, pp 21–32Google Scholar
- Lewis KR, John B (1963) Chromosome marker. Little, Brown and Company, BostonGoogle Scholar
- Matsubara K, Knopp T, Sarre SD, Georges A, Ezaz T (2013) 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). Mol Cytogenet 6:60CrossRefPubMedPubMedCentralGoogle Scholar
- Matsubara K, O’Meally D, Azad B, Georges A, Sarre S, Graves JM, Matsuda Y, Ezaz T (2015) Amplification of microsatellite repeat motifs is associated with the evolutionary differentiation and heterochromatinization of sex chromosomes in Sauropsida. Chromosoma:1–13Google Scholar
- Palacios-Gimenez OM, Marti DA, Cabral-de-Mello DC (2015a) Neo-sex chromosomes of Ronderosia bergi: insight into the evolution of sex chromosomes in grasshoppers. Chromosoma 124:353–365Google Scholar
- Rovatsos M, Pokorná M, Altmanová M, Kratochvíl L (2014b) Cretaceous park of sex determination: sex chromosomes are conserved across iguanas. Biol Lett 10Google Scholar
- Sharma GP, Kaur P, Nakhasi U (1975) Female heterogamety in the Indian cryptodiran chelonian, Kachuga smithi Gray. In: Tiwari KK, Srivistava CB (eds) Dr BS Chuahah commemoration volume. Zoological Society of India, Orissa, pp 359–368Google Scholar
- Solari AJ (1994) Sex chromosomes and sex determination in vertebrates. CRC Press, Inc., Boca RatonGoogle Scholar
- Tree of Sex C (2014) Tree of Sex: a database of sexual systems. Scientific data 1Google Scholar
- Valenzuela N, Lance VA (eds) (2004) Temperature dependent sex determination in vertebrates. Smithsonian Books, WashingtonGoogle Scholar
- Valenzuela N, Badenhorst D, Montiel Jiménez EE, Literman R (2014) Molecular cytogenetic search for cryptic sex chromosomes in painted turtles Chrysemys picta. Cytogenet Genome Res 144: 39–46Google Scholar
- van Dijk PP, Iverson JB, Rhodin AGJ, Shaffer HB, Baur B (2014) Turtles of the world, 7th edition: annotated checklist of taxonomy, synonymy, distribution with maps, and conservation status. Chelonian Res Monogr:329–479Google Scholar
- Wang J, Na J-K, Yu Q, Gschwend AR, Han J, Zeng F, Aryal R, VanBuren R, Murray JE, Zhang W, Navajas-Perez R, Feltus FA, Lemke C, Tong EJ, Chen C, Wai CM, Singh R, Wang M-L, Min XJ, Alam M, Charlesworth D, Moore PH, Jiang J, Paterson AH, Ming R (2012) Sequencing papaya X and Y-h chromosomes reveals molecular basis of incipient sex chromosome evolution. PNAS 109:13710–13715CrossRefPubMedPubMedCentralGoogle Scholar