Abstract
Hybrid sterility is a common postzygotic reproductive isolation mechanism that appears in the early stages of speciation of various organisms. Mus musculus musculus and Mus musculus domesticus 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.
Similar content being viewed by others
References
JA Blake JE Richardson CJ Bult JA Kadin JT Eppig (2003) ArticleTitleMGD: the Mouse Genome Database Nucleic Acids Res 31 193–195 Occurrence Handle10.1093/nar/gkg047 Occurrence Handle1:CAS:528:DC%2BD3sXhvFSntLY%3D Occurrence Handle12519980
P Boursot W Din R Anand D Darviche B Dod et al. (1996) ArticleTitleOrigin and radiation of the house mouse: Mitochondrial DNA phylogeny J Evol Biol 9 391–415 Occurrence Handle1:CAS:528:DyaK28XltlahtLw%3D
JA Coyne HA Orr (1989) Two rules of speciation D Otte J Endler (Eds) In Speciation and Its Consequences Sinauer Sunderland, MA 180–207
W Dietrich J Miller R Steen M Merchant D Damron et al. (1994) ArticleTitleA genetic map of the mouse with 4,006 simple sequence length polymorphisms Nat Genet 7 220–245 Occurrence Handle1:CAS:528:DyaK2cXksFWhsL4%3D Occurrence Handle7920646
B Dod L Jermiin P Boursot V Chapman J Tonnes–Nielsen et al. (1993) ArticleTitleCounterselection on sex chromosomes in the Mus musculus European hybrid zone J Evol Biol 6 529–546
R Elliott D Miller R Pearsall C Hohman Y Zhang et al. (2001) ArticleTitleGenetic analysis of testis weight and fertility in an interspecies hybrid congenic strain for Chromosome X Mamm Genome 12 45–51 Occurrence Handle10.1007/s003350010234 Occurrence Handle1:CAS:528:DC%2BD3MXptlGqug%3D%3D Occurrence Handle11178743
J Forejt (1982) X-Y involvement in male sterility caused by autosome translocations—a hypothesis M Fraccaro B, Rubin (Eds) Genetic Control of Gamete Production and Function Academic Press New York pp 135–151
J Forejt (1996) ArticleTitleHybrid sterility in the mouse Trends Genet 12 412–417 Occurrence Handle10.1016/0168-9525(96)10040-8 Occurrence Handle1:CAS:528:DyaK28Xmt12jtrc%3D Occurrence Handle8909138
J Forejt P Ivanyi (1974) ArticleTitleGenetic studies on male sterility of hybrids between laboratory and wild mice (Mus musculus L.) Genet Res 24 189–206 Occurrence Handle1:STN:280:CSqC3MzkslY%3D Occurrence Handle4452481
J Forejt V Vincek J Klein H Lehrach M Loudova–Mickova (1991) ArticleTitleGenetic mapping of the t-complex region on mouse chromosome 17 including the Hybrid sterility-1 gene Mamm Genome 1 84–91 Occurrence Handle1:CAS:528:DyaK38XkvVCntL8%3D Occurrence Handle1799792
S Gregorova J Forejt (2000) ArticleTitlePWD/Ph and PWK/Ph inbred mouse strains of Mus m. musculus subspecies—a valuable resource of phenotypic variations and genomic polymorphisms Folia Biol (Praha) 46 31–41 Occurrence Handle1:STN:280:DC%2BD3c7ptlWhsQ%3D%3D
S Gregorova M Mnukova–Fajdelova Z Trachtulec J Capkova M Loudova et al. (1996) ArticleTitleSub-milliMorgan map of the proximal part of mouse Chromosome 17 including the hybrid sterility 1 gene Mamm Genome 7 107–113 Occurrence Handle10.1007/s003359900029 Occurrence Handle1:CAS:528:DyaK28Xit1Cgt7s%3D Occurrence Handle8835526
JL Guenet C Nagamine D Simon–Chazottes X Montagutelli F Bonhomme (1990) ArticleTitleHst-3: an X-linked hybrid sterility gene Genet Res 56 163–165 Occurrence Handle1:STN:280:By6C3cnnsFE%3D Occurrence Handle2272506
IBS Haldane (1922) ArticleTitleSex ratio and unisexual sterility in animal hybrids J Genet 12 101–109
M Hemberger R Pearsall U Zechner A Orth S Otto et al. (1999) ArticleTitleGenetic dissection of X-linked interspecific hybrid placental dysplasia in congenic mouse strains Genetics 153 383–390 Occurrence Handle1:CAS:528:DyaK1MXmsVWqtbc%3D Occurrence Handle10471720
T Hubbard D Barker E Birney G Cameron Y Chen et al. (2002) ArticleTitleThe Ensembl genome database project Nucleic Acids Res 30 38–41 Occurrence Handle10.1093/nar/30.1.38 Occurrence Handle1:CAS:528:DC%2BD38Xht12ksbY%3D Occurrence Handle11752248
E Lifschytz DL Lindsley (1972) ArticleTitleThe role of X-chromosome inactivation during spermatogenesis (Drosophila-allocycly-chromosome evolution-male sterility-dosage compensation) Proc Natl Acad Sci USA 69 182–186 Occurrence Handle1:STN:280:CS2D1MvivFY%3D Occurrence Handle4621547
KF Manly RH Cudmore SuffixJr JM Meer (2001) ArticleTitleMap Manager QTX, cross-platform software for genetic mapping Mamm Genome 12 930–932 Occurrence Handle10.1007/s00335-001-1016-3 Occurrence Handle1:CAS:528:DC%2BD3MXosFGgtbo%3D Occurrence Handle11707780
X Montagutelli R Turner JH Nadeau (1996) ArticleTitleEpistatic control of non-Mendelian inheritance in mouse interspecific crosses Genetics 143 1739–1752 Occurrence Handle1:STN:280:ByiD3c7htlQ%3D Occurrence Handle8844160
HJ Muller (1940) Bearing of the Drosophila work on systematics JS Huxley (Eds) The New Systematics Clarendon Oxford 185–268
P Munclinger P Boursot B Dod (2003) ArticleTitleB1 insertions as easy markers for mouse population studies Mamm Genome 14 359–366 Occurrence Handle10.1007/s00335-002-3065-7 Occurrence Handle1:CAS:528:DC%2BD3sXltFGnsro%3D Occurrence Handle12879357
MA Noor KL Grams LA Bertucci J Reiland (2001) ArticleTitleChromosomal inversions and the reproductive isolation of species Proc Natl Acad Sci USA 98 12084–12088 Occurrence Handle10.1073/pnas.221274498 Occurrence Handle1:CAS:528:DC%2BD3MXns1CjsLo%3D Occurrence Handle11593019
HA Orr DC Presgraves (2000) ArticleTitleSpeciation by postzygotic isolation: forces, genes and molecules Bioessays 22 1085–1094 Occurrence Handle10.1002/1521-1878(200012)22:12<1085::AID-BIES6>3.3.CO;2-7 Occurrence Handle1:CAS:528:DC%2BD3MXmslWmtbg%3D Occurrence Handle11084624
J Peknicova J Moos (1990) ArticleTitleMonoclonal antibodies against boar acrosomal antigens labelling undamaged acrosomes of spermatozoa in immunofluorescence test Andrologia 22 427–435 Occurrence Handle1:STN:280:By6C2MfhtVM%3D Occurrence Handle2073053
J Peknicova V Kyselova D Buckiova M Boubelik (2002) ArticleTitleEffect of an endocrine disrupter on mammalian fertility. Application of monoclonal antibodies against sperm proteins as markers for testing sperm damage Am J Reprod Immunol 47 311–318 Occurrence Handle10.1034/j.1600-0897.2002.01112.x Occurrence Handle12148547
R Sage W Atchley E Capanna (1993) ArticleTitleHouse mice as models in systematic biology Syst Biol 42 523–561
J She F Bonhomme P Boursot L Thaler F Catzeflis (1990) ArticleTitleMolecular phylogenies in the genus Mus: Comparative analysis of electrophoretic, scnDNA hybridization, and mtDNA RFLP data Biol J Linn Soc Lond 41 83–103
L Silver (1995) Mouse Genetics. Concepts and Applications Oxford University Press Oxford, New York
N Takagi M Tada M Shoji K Moriwaki (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 K Moriwaki T Shiroishi H Yonekawa (Eds) Genetics in wild mice. Its application to biomedical research Gentics in wild mice. Its application to biomedical research . 247–256
Z Trachtulec M Mnukova–Fajdelova R Hamvas S Gregorova W Mayer et al. (1997) ArticleTitleIsolation of candidate hybrid sterility 1 genes by cDNA selection in a 1.1 megabase pair region on mouse chromosome 17 Mamm Genome 8 312–316 Occurrence Handle10.1007/s003359900430 Occurrence Handle1:CAS:528:DyaK2sXjtVOhsLc%3D Occurrence Handle9107673
P Tucker R Sage J Warner A Wilson E Eicher (1992a) ArticleTitleAbrupt cline for sex chromosomes in a hybrid zone between two species of mice Evolution 46 1146–1163
PK Tucker BK Lee BL Lundrigan EM Eicher (1992b) ArticleTitleGeographic origin of the Y chromosomes in “old” inbred strains of mice Mamm Genome 3 254–261 Occurrence Handle1:CAS:528:DyaK38Xlt1Gksr8%3D
M Turelli HA Orr (1995) ArticleTitleThe dominance theory of Haldane’s rule Genetics 140 389–402 Occurrence Handle1:STN:280:ByqA283gtlE%3D Occurrence Handle7635302
JM Turner SK Mahadevaiah DJ Elliott HJ Garchon JR Pehrson et al. (2002) ArticleTitleMeiotic sex chromosome inactivation in male mice with targeted disruptions of Xist J Cell Sci 115 4097–4105 Occurrence Handle10.1242/jcs.00111 Occurrence Handle1:CAS:528:DC%2BD38XovFOltLs%3D Occurrence Handle12356914
CM Wade EJ Kulbokas Suffix3rd AW Kirby MC Zody JC Mullikin et al. (2002) ArticleTitleThe mosaic structure of variation in the laboratory mouse genome Nature 420 574–578 Occurrence Handle10.1038/nature01252 Occurrence Handle1:CAS:528:DC%2BD38Xpt1WhsL4%3D Occurrence Handle12466852
GA Walling PM Visscher CS Haley (1998) ArticleTitleA comparison of bootstrap methods to construct confidence intervals in QTL mapping Genet Res 71 171–180 Occurrence Handle10.1017/S0016672398003164
RH Waterston K Lindblad–Toh E Birney J Rogers JF Abril et al. (2002) ArticleTitleInitial sequencing and comparative analysis of the mouse genome Nature 420 520–562 Occurrence Handle10.1038/nature01262 Occurrence Handle12466850
CI Wu CT Ting (2004) ArticleTitleGenes and speciation Nat Rev Genet 5 114–122 Occurrence Handle10.1038/nrg1269 Occurrence Handle1:CAS:528:DC%2BD2cXovV2mug%3D%3D Occurrence Handle14735122
H Yonekawa K Moriwaki O Gotoh J Watanabe J Hayashi et al. (1980) ArticleTitleRelationship between laboratory mice and subspecies Mus musculus domesticus based on restriction endonuclease cleavage patterns of mitochondrial DNA Jpn J Genet 55 289–296
KK Youngren JH Nadeau A Matin (2003) ArticleTitleTesticular cancer susceptibility in the 129. MOLF-Chr 19 mouse strain additive effects, gene interactions and epigenetic modifications Hum Mol Genet 12 389–398 Occurrence Handle10.1093/hmg/ddg036 Occurrence Handle1:CAS:528:DC%2BD3sXitVWqsLg%3D Occurrence Handle12566386
U Zechner M Reule A Orth F Bonhomme B Strack et al. (1996) ArticleTitleAn X-chromosome linked locus contributes to abnormal placental development in mouse interspecific hybrid Nat Genet 12 398–403 Occurrence Handle1:CAS:528:DyaK28XjtFaisr4%3D Occurrence Handle8630493
Acknowledgments
We thank Michael W. Nachman for permission to cite the unpublished data and Zdenek Trachtulec and Sarka Takacova for valuable comments on the manuscript. The work was supported by EU grant QLRI-2000-00233 and the Grant Agency of the Czech Republic, Grant 204/02/1373. Jiri Forejt is supported as an International Scholar of the Howard Hughes Medical Institute.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Storchová, R., Gregorová, S., Buckiová, D. et al. Genetic analysis of X-linked hybrid sterility in the house mouse. Mamm Genome 15, 515–524 (2004). https://doi.org/10.1007/s00335-004-2386-0
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/s00335-004-2386-0