Mammalian Genome

, Volume 15, Issue 7, pp 515–524

Genetic analysis of X-linked hybrid sterility in the house mouse

  • Radka Storchová
  • Soňa Gregorová
  • Daniela Buckiová
  • Vendula Kyselová
  • Petr Divina
  • Jiří Forejt
Original Contributors

Abstract

Hybrid sterility is a common postzygotic reproductive isolation mechanism that appears in the early stages of speciation of various organisms. Musmusculusmusculus and Musmusculusdomesticus represent two recently separated mouse subspecies particularly suitable for genetic studies of hybrid sterility. Here we show that the introgression of Chr X of M. m. musculus origin (PWD/Ph inbred strain, henceforth PWD) into the genetic background of the C57BL/6J (henceforth B6) inbred strain (predominantly of M. m. domesticus origin) causes male sterility. The X-linked hybrid sterility is associated with reduced testes weight, lower sperm count, and morphological abnormalities of sperm heads. The analysis of recombinant Chr Xs in sterile and fertile males as well as quantitative trait locus (QTL) analysis of several fertility parameters revealed an oligogenic nature of the X-linked hybrid sterility. The Hstx1 locus responsible for male sterility was mapped near DXMit119 in the central part of Chr X. To ensure full sterility, the PWD allele of Hstx1 has to be supported with the PWD allelic form of loci in at least one proximal and/or one distal region of Chr X. Mapping and cloning of Hstx1 and other genes responsible for sterility of B6–XPWDYB6 males could help to elucidate the special role of Chr X in hybrid sterility and consequently in speciation.

References

  1. Blake, JA, Richardson, JE, Bult, CJ, Kadin, JA, Eppig, JT 2003MGD: the Mouse Genome DatabaseNucleic Acids Res31193195CrossRefPubMedGoogle Scholar
  2. Boursot, P, Din, W, Anand, R, Darviche, D, Dod, B,  et al. 1996Origin and radiation of the house mouse: Mitochondrial DNA phylogenyJ Evol Biol9391415Google Scholar
  3. Coyne, JA, Orr, HA 1989

    Two rules of speciation

    Otte, DEndler, J eds. In Speciation and Its ConsequencesSinauerSunderland, MA180207
    Google Scholar
  4. Dietrich, W, Miller, J, Steen, R, Merchant, M, Damron, D,  et al. 1994A genetic map of the mouse with 4,006 simple sequence length polymorphismsNat Genet7220245PubMedGoogle Scholar
  5. Dod, B, Jermiin, L, Boursot, P, Chapman, V, Tonnes–Nielsen, J,  et al. 1993Counterselection on sex chromosomes in the Mus musculus European hybrid zoneJ Evol Biol6529546Google Scholar
  6. Elliott, R, Miller, D, Pearsall, R, Hohman, C, Zhang, Y,  et al. 2001Genetic analysis of testis weight and fertility in an interspecies hybrid congenic strain for Chromosome XMamm Genome124551CrossRefPubMedGoogle Scholar
  7. Forejt, J 1982

    X-Y involvement in male sterility caused by autosome translocations—a hypothesis

    Fraccaro, MRubin, B, eds. Genetic Control of Gamete Production and FunctionAcademic PressNew Yorkpp 135151
    Google Scholar
  8. Forejt, J 1996Hybrid sterility in the mouseTrends Genet12412417[erratum: Trends Genet 1997 Jan; 13(1):42]CrossRefPubMedGoogle Scholar
  9. Forejt, J, Ivanyi, P 1974Genetic studies on male sterility of hybrids between laboratory and wild mice (Mus musculus L.)Genet Res24189206PubMedGoogle Scholar
  10. Forejt, J, Vincek, V, Klein, J, Lehrach, H, Loudova–Mickova, M 1991Genetic mapping of the t-complex region on mouse chromosome 17 including the Hybrid sterility-1 geneMamm Genome18491PubMedGoogle Scholar
  11. Gregorova, S, Forejt, J 2000PWD/Ph and PWK/Ph inbred mouse strains of Mus m. musculus subspecies—a valuable resource of phenotypic variations and genomic polymorphismsFolia Biol (Praha)463141Google Scholar
  12. Gregorova, S, Mnukova–Fajdelova, M, Trachtulec, Z, Capkova, J, Loudova, M,  et al. 1996Sub-milliMorgan map of the proximal part of mouse Chromosome 17 including the hybrid sterility 1 geneMamm Genome7107113CrossRefPubMedGoogle Scholar
  13. Guenet, JL, Nagamine, C, Simon–Chazottes, D, Montagutelli, X, Bonhomme, F 1990Hst-3: an X-linked hybrid sterility geneGenet Res56163165PubMedGoogle Scholar
  14. Haldane, IBS 1922Sex ratio and unisexual sterility in animal hybridsJ Genet12101109Google Scholar
  15. Hemberger, M, Pearsall, R, Zechner, U, Orth, A, Otto, S,  et al. 1999Genetic dissection of X-linked interspecific hybrid placental dysplasia in congenic mouse strainsGenetics153383390PubMedGoogle Scholar
  16. Hubbard, T, Barker, D, Birney, E, Cameron, G, Chen, Y,  et al. 2002The Ensembl genome database projectNucleic Acids Res303841CrossRefPubMedGoogle Scholar
  17. Lifschytz, E, Lindsley, DL 1972The role of X-chromosome inactivation during spermatogenesis (Drosophila-allocycly-chromosome evolution-male sterility-dosage compensation)Proc Natl Acad Sci USA69182186PubMedGoogle Scholar
  18. Manly, KF, Cudmore, RH,Jr, Meer, JM 2001Map Manager QTX, cross-platform software for genetic mappingMamm Genome12930932CrossRefPubMedGoogle Scholar
  19. Montagutelli, X, Turner, R, Nadeau, JH 1996Epistatic control of non-Mendelian inheritance in mouse interspecific crossesGenetics14317391752PubMedGoogle Scholar
  20. Muller, HJ 1940

    Bearing of the Drosophila work on systematics

    Huxley, JS eds. The New SystematicsClarendonOxford185268
    Google Scholar
  21. Munclinger, P, Boursot, P, Dod, B 2003B1 insertions as easy markers for mouse population studiesMamm Genome14359366CrossRefPubMedGoogle Scholar
  22. Noor, MA, Grams, KL, Bertucci, LA, Reiland, J 2001Chromosomal inversions and the reproductive isolation of speciesProc Natl Acad Sci USA981208412088CrossRefPubMedGoogle Scholar
  23. Orr, HA, Presgraves, DC 2000Speciation by postzygotic isolation: forces, genes and moleculesBioessays2210851094CrossRefPubMedGoogle Scholar
  24. Peknicova, J, Moos, J 1990Monoclonal antibodies against boar acrosomal antigens labelling undamaged acrosomes of spermatozoa in immunofluorescence testAndrologia22427435PubMedGoogle Scholar
  25. Peknicova, J, Kyselova, V, Buckiova, D, Boubelik, M 2002Effect of an endocrine disrupter on mammalian fertility. Application of monoclonal antibodies against sperm proteins as markers for testing sperm damageAm J Reprod Immunol47311318CrossRefPubMedGoogle Scholar
  26. Sage, R, Atchley, W, Capanna, E 1993House mice as models in systematic biologySyst Biol42523561Google Scholar
  27. She, J, Bonhomme, F, Boursot, P, Thaler, L, Catzeflis, F 1990Molecular phylogenies in the genus Mus: Comparative analysis of electrophoretic, scnDNA hybridization, and mtDNA RFLP dataBiol J Linn Soc Lond4183103Google Scholar
  28. Silver, L 1995Mouse Genetics. Concepts and ApplicationsOxford University PressOxford, New YorkGoogle Scholar
  29. Takagi, N, Tada, M, Shoji, M, Moriwaki, K 1994

    An X-linked gene governing sperm morphology revealed in laboratory mice consomic for X chromosome from Japanese house mouse, Mus musculus molossinus Scientific Societies Press/Karger Tokyo, Basel: Japan

    Moriwaki, KShiroishi, TYonekawa, H eds. Genetics in wild mice. Its application to biomedical researchGentics in wild mice. Its application to biomedical research.247256
    Google Scholar
  30. Trachtulec, Z, Mnukova–Fajdelova, M, Hamvas, R, Gregorova, S, Mayer, W,  et al. 1997Isolation of candidate hybrid sterility 1 genes by cDNA selection in a 1.1 megabase pair region on mouse chromosome 17Mamm Genome8312316CrossRefPubMedGoogle Scholar
  31. Tucker, P, Sage, R, Warner, J, Wilson, A, Eicher, E 1992aAbrupt cline for sex chromosomes in a hybrid zone between two species of miceEvolution4611461163Google Scholar
  32. Tucker, PK, Lee, BK, Lundrigan, BL, Eicher, EM 1992bGeographic origin of the Y chromosomes in “old” inbred strains of miceMamm Genome3254261Google Scholar
  33. Turelli, M, Orr, HA 1995The dominance theory of Haldane’s ruleGenetics140389402PubMedGoogle Scholar
  34. Turner, JM, Mahadevaiah, SK, Elliott, DJ, Garchon, HJ, Pehrson, JR,  et al. 2002Meiotic sex chromosome inactivation in male mice with targeted disruptions of XistJ Cell Sci11540974105CrossRefPubMedGoogle Scholar
  35. Wade, CM, Kulbokas, EJ,3rd, Kirby, AW, Zody, MC, Mullikin, JC,  et al. 2002The mosaic structure of variation in the laboratory mouse genomeNature420574578CrossRefPubMedGoogle Scholar
  36. Walling, GA, Visscher, PM, Haley, CS 1998A comparison of bootstrap methods to construct confidence intervals in QTL mappingGenet Res71171180CrossRefGoogle Scholar
  37. Waterston, RH, Lindblad–Toh, K, Birney, E, Rogers, J, Abril, JF,  et al. 2002Initial sequencing and comparative analysis of the mouse genomeNature420520562CrossRefPubMedGoogle Scholar
  38. Wu, CI, Ting, CT 2004Genes and speciationNat Rev Genet5114122CrossRefPubMedGoogle Scholar
  39. Yonekawa, H, Moriwaki, K, Gotoh, O, Watanabe, J, Hayashi, J,  et al. 1980Relationship between laboratory mice and subspecies Mus musculus domesticus based on restriction endonuclease cleavage patterns of mitochondrial DNAJpn J Genet55289296Google Scholar
  40. Youngren, KK, Nadeau, JH, Matin, A 2003Testicular cancer susceptibility in the 129. MOLF-Chr 19 mouse strain additive effects, gene interactions and epigenetic modificationsHum Mol Genet12389398CrossRefPubMedGoogle Scholar
  41. Zechner, U, Reule, M, Orth, A, Bonhomme, F, Strack, B,  et al. 1996An X-chromosome linked locus contributes to abnormal placental development in mouse interspecific hybridNat Genet12398403PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • Radka Storchová
    • 1
    • 2
  • Soňa Gregorová
    • 1
    • 2
  • Daniela Buckiová
    • 3
  • Vendula Kyselová
    • 1
  • Petr Divina
    • 1
    • 2
  • Jiří Forejt
    • 1
    • 2
  1. 1.Institute of Molecular Genetics AS CRPragueCzech Republic
  2. 2.Centre of Integrated GenomicsPragueCzech Republic
  3. 3.Institute of Experimental Medicine Academy of Sciences of the Czech RepublicPragueCzech Republic

Personalised recommendations