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Multiple independent evolutionary losses of XY pairing at meiosis in the grey voles

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Abstract

In many eutherian mammals, X–Y chromosome pairing and recombination is required for meiotic progression and correct sex chromosome disjunction. Arvicoline rodents present a notable exception to this meiotic rule, with multiple species possessing asynaptic sex chromosomes. Most asynaptic vole species belong to the genus Microtus sensu lato. However, many of the species both inside and outside the genus Microtus display normal X–Y synapsis at meiosis. These observations suggest that the synaptic condition was present in the common ancestor of all voles, but gaps in current taxonomic sampling across the arvicoline phylogeny prevent identification of the lineage(s) along which the asynaptic state arose. In this study, we use electron and immunofluorescent microscopy to assess heterogametic sex chromosome pairing in 12 additional arvicoline species. Our sample includes ten species of the tribe Microtini and two species of the tribe Lagurini. This increased breadth of sampling allowed us to identify asynaptic species in each major Microtine lineage. Evidently, the ability of the sex chromosomes to pair and recombine in male meiosis has been independently lost at least three times during the evolution of Microtine rodents. These results suggest a lack of evolutionary constraint on X–Y synapsis in Microtini, hinting at the presence of alternative molecular mechanisms for sex chromosome segregation in this large mammalian tribe.

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Abbreviations

BSA:

Bovine serum albumin

Cy3:

Orange fluorescing cyanine

DAPI:

4′-6-Diamidino-2-phenylindole

EM:

Electron microscopy

FITC:

Fluorescein isothiocyanate

FM:

Fluorescent microscopy

MLH1:

Homolog of prokaryotic mutL 1 mismatch repair protein

SC:

Synaptonemal complex

SCP3:

Synaptonemal complex protein 3

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Acknowledgments

This work was supported by research grants from Russian Foundation for Basic Research (to PMB, EAB, AAT, OAD, FNG, IVK), Siberian and Far Eastern Departments of Russian Academy of Sciences (to PMB and IVK), National Science Foundation Predoctoral Fellowship (to BLD), and Japan Science Society Sasagawa Scientific Research Grant (to KM). We thank Mrs. Marina Rodionova for her help in SC spreading; Drs. Andrei Dobrotvorsky, Victor Panov, Yuichi Narita, Bruce Cushing, Nancy Cushing, and Ms. Roni Yi-Ju Chen for providing of animals; Drs. Sen-ichi Oda, Kazuhiro Koyasu, Masashi Harada, and Vladimir Lebedev for valuable advices; and the Microscopic Center of the Siberian Department of Russian Academy of Sciences for granting access to microscopic equipment.

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Authors and Affiliations

  1. Institute of Cytology and Genetics, Russian Academy of Sciences, Siberian Department, Novosibirsk, 630090, Russia

    Pavel M. Borodin, Ekaterina A. Basheva, Anna A. Torgasheva & Olesya A. Dashkevich

  2. Department of Cytology and Genetics, Novosibirsk State University, Novosibirsk, Russia

    Pavel M. Borodin & Olesya A. Dashkevich

  3. Zoological Institute, Russian Academy of Sciences, Sankt-Petersburg, 199034, Russia

    Ekaterina A. Basheva & Fedor N. Golenishchev

  4. Institute of Biology and Soil Science, Russian Academy of Sciences, Far Eastern Department, Vladivostok, 690022, Russia

    Irina V. Kartavtseva

  5. Experimental Animal Division, RIKEN BioResource Center, Tsukuba-shi, Ibaraki, 305-0074, Japan

    Kazuyuki Mekada

  6. Department of Genome Sciences, University of Washington, Seattle, WA, 98195-5065, USA

    Beth L. Dumont

Authors
  1. Pavel M. Borodin
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  2. Ekaterina A. Basheva
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  3. Anna A. Torgasheva
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  4. Olesya A. Dashkevich
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  5. Fedor N. Golenishchev
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  6. Irina V. Kartavtseva
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  7. Kazuyuki Mekada
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  8. Beth L. Dumont
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Correspondence to Pavel M. Borodin.

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Responsible Editor: Herbert Macgregor.

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Borodin, P.M., Basheva, E.A., Torgasheva, A.A. et al. Multiple independent evolutionary losses of XY pairing at meiosis in the grey voles. Chromosome Res 20, 259–268 (2012). https://doi.org/10.1007/s10577-011-9261-0

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  • DOI: https://doi.org/10.1007/s10577-011-9261-0

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