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.
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