The role of the x chromosome in house mouse speciation

Evolution of the House Mouse

Volumn , Issue , 2012, Pages 431-454

  Oka, Ayako ^a,b   Shiroishi, Toshihiko ^b  

^a NATIONAL INSTITUTE OF GENETICS   (Japan)

^b NATIONAL INSTITUTE OF GENETICS   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84901297927     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1017/CBO9781139044547.019     Document Type: Chapter

References (100)

1. Bateson, W. (1909). Heredity and variation in modern lights. In Darwin and Modern Science, ed. A. Seward. Cambridge: Cambridge University Press, pp 85–101.
2. Baudat, F., Buard, J., Grey, C., et al. (2010). PRDM9 is a major determinant of meiotic recombination hotspots in humans and mice. Science, 327, 836–40.
3. Bayes, J. and Malik, H. (2009). Altered heterochromatin binding by a hybrid sterility protein in Drosophila sibling species. Science, 326, 1538–41.
4. Biddle, F., Eales, B., and Dean, W. (1994). Haldane’s rule and heterogametic female and male sterility in the mouse. Genome, 37, 198–202.
5. Bonhomme, F., Catalan, J., Britton-Davidian, J., et al. (1984). Biochemical diversity and evolution in the genus Mus. Biochemical Genetics, 22, 275–303.
6. Bonhomme, F. and Guenet, J. -L. (1996). The laboratory mouse and its wild relatives. In Genetic Variants and Strains of the Laboratory Mouse, ed. M. F. Lyon, S. Rastan, and S. D. M. Brown. Oxford: Oxford University Press, pp 1577–96.
7. Bonhomme, F., Martin, S., and Thaler, L. (1978). Hybridization between Mus musculus L. and Mus spretus Lataste under laboratory conditions. Experientia, 34, 1140–1.
8. Britton-Davidian, J., Fel-Clair, F., Lopes, J., Alibert, P., and Boursot, P. (2005). Postzygotic isolation between the two European subspecies of the house mouse: estimates from fertility patterns in wild and laboratory-bred hybrids. Biological Journal of the Linnean Society, 84, 379–93.
9. Burgoyne, P. S., Mahadevaiah, S. K., and Turner, J. M. (2009). The consequences of asyn- apsis for mammalian meiosis. Nature Reviews Genetics, 10, 207–16.
10. Chubb, C. and Nolan, C. (1987). Mouse hybrid sterility and testicular function. Biology of Reproduction, 36, 1343–8.
11. Cohen, P. E., Pollack, S. E., and Pollard, J.W. (2006). Genetic analysis of chromosome pairing, recombination, and cell cycle control during first meiotic prophase in mammals. Endocrine Reviews, 27, 398–426.
12. Coyne, J. (1992). Genetics and speciation. Nature, 355, 511–15.
13. Coyne, J. A. and Orr, H. A. (1989). Two rules of speciation. In Speciation and Its Consequences, ed. D. Otte and J. Endler. Sunderland, MA: Sinauer Associates, pp 180–207.
14. Coyne, J. A. and Orr, H. A. (2004). Speciation. Sunderland, MA: Sinauer Associates.
15. Dobzhansky, T. (1936). Studies on hybrid sterility: II. Localization of sterility factors in Drosophilapseudoobscura hybrids. Genetics, 21, 113–35.
16. Dod, B., Jermiin, L. S., Boursot, P., et al. (1993). Counterselection on sex chromosomes in the Mus musculus European hybrid zone. Journal of Evolutionary Biology, 6, 529–46.
17. Elliott, R. W., Miller, D. R., Pearsall, R. S., et al. (2001). Genetic analysis of testis weight and fertility in an interspecies hybrid congenic strain for Chromosome X. Mammalian Genome, 12, 45–51.
18. Elliott, R. W., Poslinski, D., Tabaczynski, D., Hohman, C., and Pazik, J. (2004). Loci affecting male fertility in hybrids between Mus macedonicus and C57BL/6. Mammalian Genome, 15, 704–10.
19. Emerson, J., Kaessmann, H., Betran, E., and Long, M. (2004). Extensive gene traffic on the mammalian X-chromosome. Science, 303, 537–40.
20. Ferree, P. and Barbash, D. (2009). Species-specific heterochromatin prevents mitotic chromosome segregation to cause hybrid lethality in Drosophila. PLoS Biology, 7, ei000234.
21. Ferris, S. D., Sage, R. D., and Wilson, A. C. (1982). Evidence from mtDNA sequences that common laboratory strains of inbred mice are descended from a single female. Nature, 295, i63–5.
22. Forejt, J. (1981). Hybrid sterility gene located in the T/t-H-2 supergene on chromosome 17. In Current Trends in Histocompatibility: Immunogenetic and Molecular Profiles, ed. R. Reisfeld, and S. Ferrone. London: Plenum Press, pp 103–31.
23. Forejt, J. (1996). Hybrid sterility in the mouse. Trends in Genetics, 12, 412–17.
24. Forejt, J. and Ivanyi, P. (1974). Genetic studies on male sterility of hybrids between laboratory and wild mice (Mus musculus L.). GeneticalResearch, 24, 189–206.
25. Forejt, J., Vincek, V., Klein, J., Lehrach, H., and Loudova-Mickova, M. (1991). Genetic mapping of the t-complex region on mouse chromosome 17 including the Hybrid sterility-1 gene. Mammalian Genome, 1, 84–91.
26. Frazer, K. A., Eskin, E., Kang, H.M., et al. (2007). A sequence-based variation map of 8.27 million SNPs in inbred mouse strains. Nature, 448, 1050–3.
27. Geraldes, A., Basset, P., Gibson, B., et al. (2008). Inferring the history of speciation in house mice from autosomal, X-linked, Y-linked and mitochondrial genes. Molecular Ecology, 17, 5349–63.
28. Good, J.M., Dean, M.D., and Nachman, M.W. (2008a). A complex genetic basis to X-linked hybrid male sterility between two species of house mice. Genetics, 179, 2213–28.
29. Good, J., Giger, T., Dean, M., and Nachman, M. (2010). Widespread over-expression of the X chromosome in sterile F: hybrid mice. PLoS Genetics, 6, ei00ii48.
30. Good, J. M., Handel, M. A., and Nachman, M. W. (2008b). Asymmetry and polymorphism of hybrid male sterility during the early stages of speciation in house mice. Evolution, 62, 50–65.
31. Good, J. M. and Nachman, M. W. (2005). Rates of protein evolution are positively correlated with developmental timing of expression during mouse spermatogenesis. Molecular Biology and Evolution, 22, 1044–52.
32. Gregorová, S., Divina, P., Storchová, R., et al. (2008). Mouse consomic strains: exploiting genetic divergence between Mus m. musculus and Mus m. domesticus subspecies. Genome Research, 18, 509–15.
33. Guenet, J. -L. and Bonhomme, F. (2003). Wild mice: an ever-increasing contribution to a popular mammalian model. Trends in Genetics, 19, 24-31.
34. Guénet, J. -L., Nagamine, C., Simon-Chazottes, D., Montagutelli, X., and Bonhomme, F. (1990). Hst-3: an X-linked hybrid sterility gene. Genetical Research, 56, 163–15.
35. Guo, X., Su, B., Zhou, Z., and Sha, J. (2009). Rapid evolution of mammalian X-linked testis microRNAs. BMC Genomics, 10, 97.
36. Gurbich, T. and Bachtrog, D. (2008). Gene content evolution on the X-chromosome. Current Opinion in Genetics & Development, 18, 493–8.
37. Haldane, J. B. S. (1922). Sex ratio and unisexual sterility in hybrid animals. Journal of Genetics, 12, 101–9.
38. Hale, D. W., Washburn, L. L., and Eicher, E.M. (1993). Meiotic abnormalities in hybrid mice of the C57BL/6J x Mus spretus cross suggest a cytogenetic basis for Haldane’s rule of hybrid sterility. Cytogenetics and Cell Genetics, 63, 221–34.
39. Handel, M. and Schimenti, J. (2010). Genetics of mammalian meiosis: regulation, dynamics and impact on fertility. Nature Reviews Genetics, 11, 124–36.
40. Harr, B. (2006). Genomic islands ofdifferentiation between house mouse subspecies. Genome Research, 16, 730–7.
41. Hayashi, K., Yoshida, K., and Matsui, Y. (2005). A histone H3 methyltransferase controls epigenetic events required for meiotic prophase. Nature, 438, 374–8
42. Homolka, D., Ivanek, R., Capkova, J., Jansa, P., and Forejt, J. (2007). Chromosomal rearrangement interferes with meiotic X-chromosome inactivation. Genome Research, 17, 1431–7.
43. Hunt, W. G. and Selander, R. K. (1973). Biochemical genetics of hybridisation in European house mice. Heredity, 31, 11–33.
44. Iványi, P., Vojtísková, M., Démant, P., and Micková, M. (1969). Genetic factors in the ninth linkage group influencing reproductive performance in male mice. Folia Biologica (Praha), 15, 401–21.
45. Kaku, Y., Kon, Y., Takagi, N., et al. (1995). Histological analysis of male hybrid sterility induced by the Hst-1 gene in mice. Journal of Veterinary Medical Science, 57, 973–5.
46. Khil, P., Smirnova, N., Romanienko, P., and Camerini-Otero, R. (2004). The mouse X-chromosome is enriched for sex-biased genes not subject to selection by meiotic sex chromosome inactivation. Nature Genetics, 36, 642–6.
47. Kipling, D., Wilson, H., Thomson, E., et al. (1996). Structural variation of the pseudoautosomal region between and within inbred mouse strains. Proceedings of the National Academy of Sciences of the United States of America, 93, 171–5.
48. Li, X. C., Barringer, B.C., and Barbash, D.A. (2009). The pachytene checkpoint and its relationship to evolutionary patterns of polyploidization and hybrid sterility. Heredity, 102, 24–30.
49. Lifschytz, E. and Lindsley, D. (1972). The role of X-chromosome inactivation during spermatogenesis. Proceedings of the National Academy of Sciences of the United States of America, 69, 182–6.
50. Macholan, M., Baird, S. J. E., Dufkova, P., et al. (2011). Assessing multilocus introgression patterns: a case study on the mouse X chromosome in central Europe. Evolution, 65, 1428–46.
51. Macholán, M., Munclinger, P., Sugerková, M., et al. (2007). Genetic analysis of autosomal and X-linked markers across a mouse hybrid zone. Evolution, 61, 746–71.
52. Malmanche, N., Maia, A., and Sunkel C. E. (2006). The spindle assembly checkpoint: preventing chromosome mis-segregation during mitosis and meiosis. FEBS Letters, 580, 2888–95.
53. Masly, J., Jones, C., Noor, M., Locke, J., and Orr, H. (2006). Gene transposition as a cause of hybrid sterility in Drosophila. Science, 313, 1448–50.
54. Matsuda, Y. and Chapman, V. M. (1994). X-Y chromosome pairing and hybrid sterility of mice. In Genetics in Wild Mice: Its Application to Biomedical Research, ed. K. Moriwaki, T. Shiroishi, and H. Yonekawa. Tokyo: Japan Scientific Press and Karger, pp 257–75.
55. Matsuda, Y., Hirobe, T., and Chapman, V. M. (1991). Genetic basis of X-Y chromosome dissociation and male sterility in interspecific hybrids. Proceedings ofthe National Academy of Sciences of the United States of America, 88, 4850–4.
56. Matsuda, Y., Moens, P. B., and Chapman, V. M. (1992). Deficiency ofX and Y chromosomal pairing at meiotic prophase in spermatocytes of sterile interspecific hybrids between laboratory mice (Mus domesticus) and Mus spretus. Chromosoma, 101, 483–92.
57. Mayr, E. (1942). Systematics and the Origin of Species. New York: Columbia University Press.
58. Mihola, O., Trachtulec, Z., Vlcek, C., Schimenti, J. C., and Forejt, J. (2009). A mouse speciation gene encodes a meiotic histone h3 methyltransferase. Science, 323, 373–5.
59. Morelli, M. A. and Cohen, P. E. (2005). Not all germ cells are created equal: aspects of sexual dimorphism in mammalian meiosis. Reproduction, 130, 761–81.
60. Moriwaki, K. (1994). Wild mice from the geneticist’s viewpoint. In Genetics in Wild Mice: Its Application to Biomedical Research, ed. K. Moriwaki, T. Shiroishi, and H. Yonekawa. Tokyo: Japan Scientific Press and Karger, pp viii–xxv.
61. Mueller, J. L., Mahadevaiah, S. K., Park, P. J., et al. (2008). The mouse X-chromosome is enriched for multicopy testis genes showing postmeiotic expression. Nature Genetics, 40, 794–9.
62. Muller, H. J. (1942). Isolating mechanisms, evolution and temperature. Biological Symposia, 6, 71–125.
63. Nadeau, J., Singer, J., Matin, A., and Lander, E. (2000). Analysing complex genetic traits with chromosome substitution strains. Nature Genetics, 24, 221–5.
64. Namekawa, S. H., Park, P. J., Zhang, L. F., et al. (2006). Postmeiotic sex chromatin in the male germline of mice. Current Biology, 16, 660–7.
65. Oka, A., Aoto, T., Totsuka, Y., et al. (2007). Disruption of genetic interaction between two autosomal regions and the X-chromosome causes reproductive isolation between mouse strains derived from different subspecies. Genetics, 175, 185–97.
66. Oka, A., Mita, A., Sakurai-Yamatani, N., et al. (2004). Hybrid breakdown caused by substitution of the X-chromosome between two mouse subspecies. Genetics, 166, 913–24.
67. Oka, A., Mita, A., Takada, Y., Koseki, H., and Shiroishi, T. (2010). Reproductive isolation in hybrid mice due to spermatogenesis defects at three meiotic stages. Genetics, 186, 339–51.
68. Oliver, P., Goodstadt, L., Bayes, J., et al. (2009). Accelerated evolution of the Prdmg speciation gene across diverse metazoan taxa. PLoS Genetics, 5, ei000753.
69. Orr, H. A. (1993). Haldane’s rule has multiple genetic causes. Nature, 361, 532–3.
70. Orr, H. A. (2005). The genetic basis of reproductive isolation: insights from Drosophila. Proceedings of the National Academy of Sciences ofthe United States of America, 102, 6522–6.
71. Orth, A., Belkhir, K., Britton-Davidian, J., et al. (2002). Natural hybridisation between two sympatric species of mice Mus musculus domesticus L. and Mus spretus Lataste. Comptes Rendus Biologies, 325, 89–97.
72. Payseur, B.A., Krenz, J. G., and Nachman, M.W. (2004). Differential patterns of introgression across the X-chromosome in a hybrid zone between two species of house mice. Evolution, 58, 2064–78.
73. Presgraves, D. (2003). A fine-scale genetic analysis of hybrid incompatibilities in Drosophila. Genetics, 163, 955–72.
74. Rice, W. (1984). Sex chromosomes and the evolution of sexual dimorphism. Evolution, 38, 735–42.
75. Roeder, G. S. and Bailis, J.M. (2000). The pachytene checkpoint. Trends in Genetics, 16, 395–403
76. Sakai, T., Kikkawa, Y., Miura, I., et al. (2005). Origins of mouse inbred strains deduced from whole-genome scanning by polymorphic microsatellite loci. Mammalian Genome, 16, 11–19.
77. Sawamura, K. and Yamamoto, M. (1997). Characterization of a reproductive isolation gene, zygotic hybrid rescue, of Drosophila melanogaster by using minichromosomes. Heredity, 79, 97–I03.
78. Solari, A. J. (1974). The behavior of the XY pair in mammals. International Review of Cytology, 38, 273–3i7.
79. Song, R., Ro, S., Michaels, J., et al. (2009). ManyX-linked microRNAs escape meiotic sex chromosome inactivation. Nature Genetics, 41, 488–93.
80. Storchová, R., Gregorová, S., Buckiová, D., et al. (2004). Genetic analysis ofX-linked hybrid sterility in the house mouse. Mammalian Genome, 15, 515–24.
81. Takada, T., Mita, A., Maeno, A., et al. (2008). Mouse intersubspecific consomic strains for genetic dissection of quantitative complex traits. Genome Research, 18, 500–8.
82. Tarsounas, M. and Moens, P. B. (2001). Checkpoint and DNA-repair proteins are associated with the cores of mammalian meiotic chromosomes. Current Topics in Developmental Biology, 51, 109–34.
83. Ting, C., Tsaur, S., Wu, M., and Wu, C. (1998). A rapidly evolving homeobox at the site of a hybrid sterility gene. Science, 282, 1501–4.
84. Tucker, P. K., Sage, R. D., Warner, J., Wilson, A. C., and Eicher, E. M. (1992). Abrupt cline for sex chromosomes in a hybrid zone between two species of mice. Evolution, 46, 1146–63.
85. Turelli, M. and Orr, H. A. (1995). The dominance theory of Haldane’s rule. Genetics, 143, 609–11.
86. Turelli, M. and Orr, H. A. (2000). Dominance, epistasis and the genetics of postzygotic isolation. Genetics, 154, 1663–79.
87. Turner, J. M. A. (2007). Meiotic sex chromosome inactivation. Development, 134, 1823–31.
88. Vanlerberghe, F., Boursot, P., Bellis, M., Thaler, L., and Bonhomme, F. (1986). Genetical aspect of the semi-specific interaction between Mus musculus domesticus and Mus musculus musculus in eastern Europe. Genetical Research, 47, 222–3.
89. Vicoso, B. and Charlesworth, B. (2006). Evolution on the X-chromosome: unusual patterns and processes. Nature Reviews Genetics, 7, 645–53.
90. Vyskočilová, M., Pražanová, G., and Pialek, J. (2009). Polymorphism in hybrid male sterility in wild-derived Mus musculus musculus strains on proximal chromosome 17. Mammmalian Genome, 20, 83–91.
91. Wang, P. J., McCarrey, J. R., Yang, F., and Page, D. C. (2001). An abundance ofX-linked genes expressed in spermatogonia. Nature Genetics, 27, 422–6.
92. Wolgemuth, D. J., Laurion, E., and Lele, K. M. (2002). Regulation of the mitotic and meiotic cell cycles in the male germ line. Recent Progress in Hormone Research, 57, 75–101.
93. Wu, C. and Davis, A. (1993). Evolution of postmating reproductive isolation: the composite nature of Haldane’s rule and its genetic bases. The American Naturalist, 142, 187–212.
94. Wu, C. and Xu, E. (2003). Sexual antagonism and X inactivation: the SAXI hypothesis. Trends in Genetics, 19, 243–7.
95. Yan, W. (2009). Male infertility caused by spermiogenic defects: Lessons from gene knockouts. Molecular and Cellular Endocrinology, 306, 24–32.
96. Yang, H., Wang, J. R., Didion, J. P., et al. (2011). Subspecific origin and haplotype diversity in the laboratory mouse. Nature Genetics, 43, 648–55.
97. Yin, S., Sun, X. F., Schatten, H., and Sum, Q.Y. (2008). Molecular insights into mechanisms regulating faithful chromosome separation in female meiosis. Cell Cycle, 7, 2997–3005.
98. Yonekawa, H., Moriwaki, K., Gotoh, O., et al. (1980). Relationship between laboratory mice and the subspecies Mus musculus domesticus based on restriction endonuclease cleavage sites. Japanese Journal of Genetics, 55, 289–96.
99. Yonekawa, H., Moriwaki, K., Gotoh, O., et al. (1988). Hybrid origin of Japanese mice ‘Mus musculus molossinus: evidence from restriction analysis of mitochondrial DNA. Molecular Biology and Evolution, 5, 63–78.
100. Yoshiki, A., Moriwaki, K., Sakakura, T., and Kusakabe, M. (1993). Histological studies on male sterility of hybrids between laboratory and wild mouse strains. Development, Growth and Differentiation, 35, 271–81.