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Dissection of a Y-autosome translocation in Cryptomys hottentotus (Rodentia, Bathyergidae) and implications for the evolution of a meiotic sex chromosome chain

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Abstract

We describe the outcome of a comprehensive cytogenetic survey of the common mole-rat, Cryptomys hottentotus, based on G and C banding, fluorescence in situ hybridisation and the analysis of meiotic chromosomes using immunostaining of proteins involved in the formation of synaptonemal complex (SCP1 and SCP3). We identified the presence of a Y-autosome translocation that is responsible for a fixed diploid number difference between males (2n = 53) and females (2n = 54), a character that likely defines the C. hottentotus lineage. Immunostaining, combined with C banding of spermatocytes, revealed a linearised sex trivalent with X1 at one end and X2 at the other, with evidence of reduced recombination between Y and X2 that seems to be heterochromatin dependant in the C. hottentotus lineage. We suggest that this could depict the likely initial step in the differentiation of a true neo-X, and that this may mimic an early stage in the mammalian meiotic chain formation, an evolutionary process that has been taken to an extreme in a monotreme mammal, the platypus.

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Acknowledgments

SCP antibodies were kindly provided by Christa Heyting, Wageningen University, Netherlands. Patricia O’Brien and Professor MA Ferguson-Smith (Cambridge Resource Centre for Comparative Genomics, Centre for Veterinary Science, University of Cambridge) are thanked for flow sorting the mole-rat painting probes. Funding to TJR by a South African National Research Foundation grant is gratefully acknowledged. Fred Elder provided insightful comments on an earlier draft of this manuscript.

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Correspondence to T. J. Robinson.

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Communicated by E.A. Nigg

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Supplementary Fig. 1

Double-colour FISH on C. h. natalensis metaphase chromosomes using H. glaber the chromosome painting probes HGL5+6 detected with Cy3 (in pink) and HGL23 detected with FITC (in green). The hybridised chromosomes numbers refer to the C. h. natalensis karyotype presented Fig. 1. (a) The two HGL23 signals (green) corresponds to pair 26 in the female, while in the male (b), the signal corresponds to the X2 (chromosome 26) and the translocated partner which is fused to the Y. We included the inverted DAPI-stained images to facilitate the identification of the chromosomes. The horizontal scale bars correspond to 100 μm (GIF 87 kb)

High resolutuin (TIF 909 kb)

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Deuve, J.L., Bennett, N.C., Ruiz-Herrera, A. et al. Dissection of a Y-autosome translocation in Cryptomys hottentotus (Rodentia, Bathyergidae) and implications for the evolution of a meiotic sex chromosome chain. Chromosoma 117, 211–217 (2008). https://doi.org/10.1007/s00412-007-0140-6

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