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Chromosomal speciation in mice: a cytogenetic analysis of recombination

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Abstract

Within species, populations differing by chromosomal rearrangements (“chromosomal races”) may become reproductively isolated in association with reduced hybrid fertility due to meiotic aberrations. Speciation is also possible if hybridizing chromosomal races accumulate genetic differences because of reduced meiotic recombination in the heterozygous configuration in hybrids. Here, we examine recombination in pure races and hybrids within a model system for chromosomal speciation: the hybridization of the Poschiavo (CHPO) and Upper Valtellina (IUVA) chromosomal races of house mouse in Upper Valtellina, Italy. These races differ by Robertsonian fusions/whole-arm reciprocal translocations, such that hybrids produce a pentavalent meiotic configuration. We determined the number and position of the recombination points (using an antibody against the MutL homolog 1 [MLH1] protein) on synaptonemal complexes at pachytene in laboratory-reared CHPO, IUVA, and hybrid males, analyzing at least 112 spermatocytes per karyotypic group, up to a total of 534 spermatocytes. The mean ± standard deviation numbers of MLH1 foci per spermatocyte were 22.2 ± 3.2, 20.1 ± 2.9, 20.7 ± 2.3, and 21.9 ± 2.9 for CHPO, IUVA, CHPO × IUVA, and IUVA × CHPO, respectively. Altogether, 10,146 chromosome arms were examined, allowing multiple comparisons. Overall, recombination events were more frequently distal than proximal or interstitial. The average number of proximal MLH1 foci per chromosome arm decreased going from telocentric to metacentric bivalents to pentavalents (when present), which (together with other factors) influenced the average number of MLH1 foci per cell between CHPO, IUVA, and hybrid mice. The low frequency of proximal recombination in pentavalents of CHPO–IUVA hybrids may promote reproductive isolation between the CHPO and IUVA races, when coupled with reduced hybrid unfitness.

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Abbreviations

CHPO:

Poschiavo [chromosomal race]

CIII:

Chain-of-three

CV:

Chain-of-five

CREST:

Calcinosis, Raynaud's syndrome, esophageal dysmotility, sclerodactyly, telangiectasia

DAPI:

4′,6-diamidino-2-phenylindole

F0 :

Parental generation

F1 :

First generation

IUVA:

Upper Valtellina [chromosomal race]

MLH1:

MutL homolog 1

PBS:

Phosphate-buffered saline

PBT:

Phosphate-buffered saline plus Tween-20

Rb:

Robertsonian

SC:

Synaptonemal complex

SD:

Standard deviation

SYCP3:

Synaptonemal complex protein 3

WARTs:

Whole-arm reciprocal translocations

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Acknowledgments

We acknowledge the funding from the Natural Environment Research Council. We thank the two anonymous reviewers for their very helpful comments.

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Authors and Affiliations

  1. Dipartimento di Biologia e Biotecnologie “Lazzaro Spallanzani”, University of Pavia, Via Ferrata 9, 27100, Pavia, Italy

    Valeria Merico, Chiara Vasco & Silvia Garagna

  2. Department of Biology, University of York, Wentworth Way, York, YO10 5DD, UK

    Mabel D. Giménez, Jeremy B. Searle & Heidi C. Hauffe

  3. Instituto de Biología Subtropical, Facultad de Ciencias Exactas, Químicas y Naturales, Universidad Nacional de Misiones, Félix de Azara 1552, N3300LQH, Posadas, Misiones, Argentina

    Mabel D. Giménez

  4. Unità Operativa di Patologia Clinica e Genetica Medica, Fondazione IRCCS Istituto Neurologico Carlo Besta, Milan, 20133, Italy

    Chiara Vasco

  5. Dipartimento di Scienze Biomediche, Biotecnologiche e Traslazionali (S.Bi.Bi.T.), Sezione di Anatomia, Istologia ed Embriologia, University of Parma, Parma, 43100, Italy

    Maurizio Zuccotti

  6. Department of Ecology and Evolution, Cornell University, Corson Hall, Ithaca, NY, 14853-2701, USA

    Jeremy B. Searle

  7. Department of Biodiversity and Molecular Ecology, Research and Innovation Centre, Fondazione Edmund Mach, Via E. Mach 1, 38010, San Michele all’Adige, TN, Italy

    Heidi C. Hauffe

  8. Centro di Eccellenza in Biologia Applicata e Centro di Ricerca Interdipartimentale di Ingegneria Tissutale, Università degli Studi di Pavia, Pavia, 27100, Italy

    Silvia Garagna

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  1. Valeria Merico
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  2. Mabel D. Giménez
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  3. Chiara Vasco
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  4. Maurizio Zuccotti
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  5. Jeremy B. Searle
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  6. Heidi C. Hauffe
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  7. Silvia Garagna
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Corresponding author

Correspondence to Jeremy B. Searle.

Additional information

Responsible Editor: Fengtang Yang.

Valeria Merico, Mabel D. Giménez, Chiara Vasco, Jeremy B. Searle, Heidi C. Hauffe, and Silvia Garagna contributed equally to this work.

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Merico, V., Giménez, M.D., Vasco, C. et al. Chromosomal speciation in mice: a cytogenetic analysis of recombination. Chromosome Res 21, 523–533 (2013). https://doi.org/10.1007/s10577-013-9377-5

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  • DOI: https://doi.org/10.1007/s10577-013-9377-5

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