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Viability of X-autosome translocations in mammals: an epigenomic hypothesis from a rodent case-study

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Abstract

X-autosome translocations are highly deleterious chromosomal rearrangements due to meiotic disruption, the effects of X-inactivation on the autosome, and the necessity of maintaining different replication timing patterns between the two segments. In spite of this, X-autosome translocations are not uncommon. We here focus on the genus Taterillus (Rodentia, Gerbillinae) which provides two sister lineages differing by two autosome–gonosome translocations. Despite the recent and dramatic chromosomal repatterning characterising these lineages, the X-autosome translocated species all display intercalary heterochromatic blocks (IHBs) between the autosomal and the ancestral sexual segments. These blocks, composed of highly amplified telomeric repeats and rDNA clusters, are not observed on the chromosomes of the non-translocated species, nor the Y1 and Y2 of the translocated species. Such IHBs are found in all mammals documented for X-autosome translocation. We propose an epigenomic hypothesis which explains the viability of X-autosome translocations in mammals. This posits that constitutive heterochromatin is probably selected for in X-autosome translocations since it may (1) prevent facultative heterochromatinization of the inactivated X from spreading to the autosomal part, and (2) allow for the independent regulation of replication timing of the sex and autosomal segments.

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Acknowledgements

We are grateful to J. Britton-Davidian, P.C.M. O’Brien, T.J. Robinson, K.A. Tolley and P. Waters for helpful comments on this manuscript, and to C. Canler, R. Cornette and J.P. Coutanceau for technical assistance. The suggestions made by four anonymous reviewers were greatly appreciated.

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  1. G. Dobigny

    Present address: Evolutionary Genomics Group, Department of Zoology, University of Stellenbosch, Private Bag X1, Matieland, 7602, South Africa

Authors and Affiliations

  1. Laboratoire Origine, Structure et Evolution de la Biodiversité, Muséum National d’Histoire Naturelle, 55, rue Buffon, 75005, Paris, France

    G. Dobigny & V. Volobouev

  2. Service de Systématique Moléculaire, MNHN, 57, rue Cuvier, 75005, Paris, France

    G. Dobigny, C. Ozouf-Costaz & C. Bonillo

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  1. G. Dobigny
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  2. C. Ozouf-Costaz
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  4. V. Volobouev
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Correspondence to G. Dobigny.

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Communicated by T. Hassold

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Dobigny, G., Ozouf-Costaz, C., Bonillo, C. et al. Viability of X-autosome translocations in mammals: an epigenomic hypothesis from a rodent case-study. Chromosoma 113, 34–41 (2004). https://doi.org/10.1007/s00412-004-0292-6

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