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A new cytotype of the African pygmy mouse Mus minutoides in Eastern Africa. Implications for the evolution of sex-autosome translocations

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Abstract

The African pygmy mice (genus Mus, subgenus Nannomys) are recognized for their highly conserved morphology but extensive chromosomal diversity, particularly involving sex-autosome translocations, one of the rarest chromosomal rearrangements among mammals. It has been shown that in the absence of unambiguous diagnostic morphological traits, sex-autosome translocations offer accurate taxonomic markers. For example, in Mus minutoides, irrespective of the diploid number (which ranges from 2n = 18 to 34), all specimens possess the sex-autosome translocations (X.1) and (Y.1) that are unique to this species. In this study, we describe a new cytotype that challenges this view. Males are characterized by the translocation (Y.1) only, while females carry no sex-autosome translocation, the X chromosome being acrocentric. Hence, although sex-autosome translocations (X.1) and (Y.1) are still diagnostic when one or both are present, their absence does not rule out M. minutoides. This cytotype has a large distribution, with specimens found in Tanzania and in the eastern part of South Africa. The nonpervasive distribution of Rb(X.1) provides an opportunity to investigate different evolutionary scenarios of sex-autosome translocations using a phylogenetic framework and the distribution of telomeric repeats. The results tend to support a scenario involving a reversal event, i.e., fusion then fission of Rb(X.1), and highlighted the existence of a new X1X1X2X2/X1X2Y sex chromosome system, confirming the remarkable diversity of neo-sex chromosomes and sex determination systems in the African pygmy mice.

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Abbreviations

AIC:

Akaike information criterion

DAPI:

4′,6-Diamino-2-phenylindole

DNA:

Deoxyribonucleic acid

EMBL:

European molecular biology laboratory

FISH:

Fluorescence in situ hybridization

GTR + G + I model:

General-time reversible + Gamma + proportion invariant model

ML:

Maximum likelihood

PCR:

Polymerase chain reaction

Rb fusion:

Robertsonian fusion

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Acknowledgments

This study was supported by the ANR grant “SEXYMUS” (N° 10-JCJC-1605) to FV, and the Plateforme Cytogénomique évolutive of the LabEx CeMEB. The specimens from Tanzania were collected as part of a University of Antwerp Special Fund for Research project, and those from South Africa were collected as part of a EKZN Wildlife registered project under collecting permit OP4189/2013. BB and SG are research fellows of Research Foundation Flanders (FWO). Our gratitude goes out to the staff of the Pest Management Center at the Sokoine University of Agriculture in Morogoro, Tanzania, for help with the field work.

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Authors and Affiliations

  1. Institut des Sciences de l’Evolution de Montpellier, Université Montpellier 2, UMR CNRS 5554, Montpellier, France

    F. Veyrunes, J. Perez & J. Britton-Davidian

  2. Evolutionary Ecology Group, University of Antwerp, Groenenborgerlaan 171, 2020, Antwerpen, Belgium

    B. Borremans & S. Gryseels

  3. Durban Natural Science Museum, Durban, South Africa

    L. R. Richards

  4. Evolutionary Genomics Group, Department of Botany and Zoology, University of Stellenbosch, Stellenbosch, South Africa

    A. Duran & T. J. Robinson

  5. Laboratoire de Biométrie et Biologie Evolutive, UMR CNRS 5558, Université Lyon 1, Villeurbanne, France

    P. Chevret

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  1. F. Veyrunes
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  2. J. Perez
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  3. B. Borremans
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  4. S. Gryseels
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  7. P. Chevret
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  9. J. Britton-Davidian
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Correspondence to F. Veyrunes.

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Veyrunes, F., Perez, J., Borremans, B. et al. A new cytotype of the African pygmy mouse Mus minutoides in Eastern Africa. Implications for the evolution of sex-autosome translocations. Chromosome Res 22, 533–543 (2014). https://doi.org/10.1007/s10577-014-9440-x

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