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Chromosoma

, Volume 126, Issue 1, pp 105–113 | Cite as

Discovery of the youngest sex chromosomes reveals first case of convergent co-option of ancestral autosomes in turtles

  • E. E. Montiel
  • D. Badenhorst
  • J. Tamplin
  • R. L. Burke
  • N. Valenzuela
Original Article

Abstract

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.

Keywords

Evolution 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 

Notes

Acknowledgments

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.

Supplementary material

412_2016_576_MOESM1_ESM.pdf (30 kb)
ESM 1 Gene content and relative position of Chrysemys picta (CPI) BAC clones mapped to (and tentatively assigned to) the sex chromosomes of Glyptemys insculpta (GIN). Shaded cells denote BACs involved in chromosomal inversions in G. insculpta. Wt1 gene is highlighted in yellow. (PDF 30 kb)

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Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • E. E. Montiel
    • 1
  • D. Badenhorst
    • 1
  • J. Tamplin
    • 2
  • R. L. Burke
    • 3
  • N. Valenzuela
    • 1
  1. 1.Department of Ecology, Evolution and Organismal BiologyIowa State UniversityAmesUSA
  2. 2.Department of BiologyUniversity of Northern IowaCedar FallsUSA
  3. 3.Department of BiologyHofstra UniversityHempsteadUSA

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