Meiotic drive in mice carrying t-complex in their genome

Russian Journal of Genetics

Volumn 49, Issue 9, 2013, Pages 885-897

  Safronova, L D ^a   Chubykin, V L ^b  

^a SEVERTSOV INSTITUTE OF ECOLOGY AND EVOLUTION   (Russian Federation)

^b VAVILOV INSTITUTE OF GENERAL GENETICS   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

ALLELE; CHROMOSOME; GENE LOCUS; GENETIC MODEL; GENETIC SELECTION; GENOME; HAPLOTYPE; HETEROZYGOSITY; INHERITANCE; MALE STERILITY; MEIOSIS; MOUSE; NONHUMAN; POPULATION GENETICS; PRIORITY JOURNAL; REVIEW; SPECIES DIFFERENTIATION; SPERMATOZOON;

EID: 84884253276     PISSN: 10227954     EISSN: 16083369     Source Type: Journal    
DOI: 10.1134/S1022795413060094     Document Type: Review

References (108)

1. Anglo-russkii tolkovyi slovar' geneticheskikh terminov (English-Russian Explanatory Dictionary of Genetic Terms), Aref'ev, V. A. and Lisovenko, L. A., Moscow: VNIRO, 1995.
2. Rieger, R., Michelis, A., and Green, M., Grossary of Genetics and Cytogenetics (Classical and Molecular), Jena: Gustav Fisher, 1976, pp. 348-349.
3. Sandler, L. and Novitski, E., Meiotic drive as an evolution force, Am. Nat., 1957, vol. 91, pp. 105-110.
4. Dunn, L. C. and Levene, H., Population dynamics of a variant t-alleles in a confined populations of wild house mice, Evolution, 1961, vol. 15, no. 4, pp. 385-391.
5. Silver, L. M., The peculiar journey of a selfish chromosome: mouse t haplotypes and meiotic drive, Trends Genet., 1993, vol. 9, pp. 250-254.
6. Lyttle, T. W., Cheaters sometimes prosper: distortion of Mendelian segregation by meiotic drive, Trends Genet., 1993, vol. 9, pp. 205-210.
7. Dobrovolskaia-Zavadskaia, N. and Kobozieff, N., Sur la reproduction des souris anoures, Comp. Rend. Soc. Biol., 1927, vol. 97, pp. 116-118.
8. Fox, H. S., Martin, G. R., Lyon, M., et al., Molecular probes define different regions of the mouse t complex, Cell, 1985, vol. 40, pp. 63-69.
9. Hammer, M., Schimenti, J., and Silver, L. M., Evolution of mouse chromosome 17 and origin of inversions associated with t-haplotypes, Proc. Natl. Acad. Sci. U. S. A., 1989, vol. 86, pp. 3261-3265.
10. Lyon, M. F., Transmission ratio distortion in mice, Annu. Rev. Genet., 2003, vol. 37, pp. 393-408.
11. Lyon, M., Elucidating mouse transmission ratio distortion, Nat. Genet., 2005, vol. 37, no. 9, pp. 924-925.
12. Lewontin, R. C. and Dunn, L. C., The evolutionary dynamics of polymorphism in the house mouse, Genetics, 1960, vol. 45, pp. 705-722.
13. van Boven, M. and Weissing, F. J., Evolution of segregation distortion: potential for a high degree of polymorphism, Theor. Biol., 1998, vol. 192, no. 2, pp. 131-142.
14. Bennett, D., The T-locus of the mouse, Cell, 1975, vol. 6, pp. 441-446.
15. Bennett, D., Dunn, L. C., and Artzt, K., Genetic change in mutations at the T/t-locus in the mouse, Genetics, 1976, vol. 83, no. 2, pp. 361-372.
16. Lyon, M. F., Transmission ratio distortion in mouse t-haplotypes is due to multiple distorter genes acting on a responder locus, Cell, 1984, vol. 37, pp. 621-628.
17. Lyon, M. F., Male sterility of the mouse t-complex is due to homozygosity of the distorter genes, Cell, 1986, vol. 44, pp. 357-363.
18. Silver, L. and Remis, D., Five of the nine genetically defined regions of mouse t-haplotypes are involved in transmission ratio distortion, Genet. Res., 1987, vol. 49, pp. 51-52.
19. Lyon, M. F., Zenton, J., Burteshaw, M. D., and Willison, K., Extent of the mouse t-complex and its inversions show by in situ hybridization, Immunogenetics, 1988, vol. 27, pp. 375-382.
20. Lyon, M. F., Deletion of mouse t-complex an effect like that of the t-form of the distorter, Genet. Res., 1992, vol. 59, pp. 27-33.
21. Uehara, H., Ebersole, T., Bennett, D., and Artzt, K., Submegabase clusters of unstable tandem repeats unique to the Tla region of mouse t haplotypes, Genetics, 1999, no. 126, pp. 1093-1102.
22. Herrmann, B. G., Koschorz, B., Wertz, K., et al., A protein kinase encoded by the t complex responder gene causes non-Mendelian inheritance, Nature, 1999, vol. 11, no. 402 (6758), pp. 141-146.
23. Bauer, H., Willert, J., Koschorz, B., and Herrmann, B. G., The t complex-encoded GTPase-activating protein TAGAP1 acts as a transmission ratio distorter in mice, Nat. Genet., 2005, vol. 37, pp. 969-973.
24. Bauer, H., Veron, N., Willert, J., and Herrmann, B. G., The t complex-encoded guanine nucleotide exchange factor Fgd2 reveals that two opposing signaling pathways promote transmission ratio distortion in the mouse, Development, 2007, vol. 21, pp. 143-147.
25. Erhart, M. A., Phillips, S. J., Bonhomomme, F., et al., t Haplotypes that are mosaic for wild-type and t-complex in wild mice, Genetics, 1989, vol. 12, pp. 405-415.
26. Erhart, M. A., Lekgothoane, S., Grenier, J., and Nadeau, J. H., Pattern of segmental recombination in theistal inversion of mouse t haplotypes, Mamm. Genome, 2002, vol. 13, no. 8, pp. 438-444.
27. Baker, A. E. M., The role of deme size, reproductive patterns and dispersal in dynamics of lethal t haplotypes, Evolution, 1993, vol. 47, pp. 1342-1359.
28. Baker, A. E. M., Mendelian inheritance of t haplotypes in house mouse (Mus musculus domesticus) gield populations, Genet. Res., 2008, vol. 90, no. 4, pp. 331-339.
29. Planchart, A. Y. and Schimenti, J. C., Physical mapping of male fertility and meiotic drive quantitative trait loci in the mouse t complex using chromosome deficiencies, Genetics, 2000, vol. 155, no. 2, pp. 803-812.
30. Fraser, L. R., and Dudley, K., New insights into the t-complex and control of sperm function, BioEssays, 1999, vol. 21, no. 4,. pp. 304-312.
31. Olds-Clarke, P., Sperm from tw32/+ mice: capacitation is normal, but hyperactivation is premature and non-hyperactivated sperm are slow, Dev. Biol., 1989, vol. 131, pp. 475-482.
32. King, S. M., Dillman, J. F., Benashski, S. E., et al., The mouse t-complex-encoded protein TCTEX1 is a light chain of brain cytoplasmic dynein, J. Biol. Chem., 1996, vol. 271, pp. 32281-32287.
33. Patel-King, R. S., Benashski, S. E., Harrison, A., and King, S. M., A Chlamydomonas homologue of the putative murine t complex distorter Tctex2 is an outer arm dynein light chain, J. Cell Biol., 1997, vol. 170, pp. 183-194.
34. Lader, E., O'Neill, M. J., Artzt, H., and Bennett, D., Tctex1: a candidate gene family for a mouse t complex sterility locus, Cell, 1989, vol. 58, pp. 969-979.
35. Huw, L. Y., Goldsborough, A. S., Willison, K., and Artzt, K., Tctex2: a sperm tail surface protein mapping to the t-complex in the promoter of Tctex-1, Development, 1995, vol. 121, pp. 561-568.
36. Inaba, K., Kagami, O., and Ogawa, K., Tctex2-related outer arm dynein light chain is phosphorylated at activation of sperm motility, Biochem. Biophys. Res. Commun., 1999, vol. 5, no. 256, pp. 177-183.
37. Pilder, S. H., Olds-Clarke, P., Phillips, D. M., and Silver, L. M., Hybrid sterility-6: a mouse t complex locus controlling sperm flagellar assembly and movement, Dev. Biol., 1993, vol. 159, pp. 631-642.
38. Pilder, S. H., Lu, J., Han, Y., et al., The molecular basis of curlicue a sperm motility abnormality linked to the sterility of t haplotype homozygous male mice, Soc. Refrodd. Fertile, 2007, vol. 63, suppl., pp. 123-139.
39. Hui, L., Lu, J., Han, Y., and Pilder, S. H., The mouse t complex gene Tsga2, encoding polypeptides located in the sperm tail and anterior acrosome, maps to locus associated with sperm motility and sperm-egg interaction abnormalities, Biol. Reprod., 2006, vol. 74, no. 4, pp. 633-643.
40. Pazour, G. J., Koutoulis, A., and Benashski, S. E., LC2, the Chlamydomonas homologue of the t complex-encoded protein TCTEX2, is essential for outer dynein arm assembly, Mol. Biol. Cell, 1999, vol. 10, pp. 3507-3520.
41. Ardlie, K. G. and Silver, L. M., Recent evolution of mouse t-haplotypes at polymorphic microsatellites associated with the t complex responder (Tcr) locus, Genet. Res., 1996, vol. 67, pp. 1-10.
42. Ardlie, K. G. and Silver, L., Low frequency of t haplotypes in natural populations of house mice (Mus musculus domesticus), Evolution, 1998, vol. 52, pp. 1185-1196.
43. Dod, B., Lithel, C., Makoundou, P., et al., Identification and characterization of t-haplotypes in wild mice populations using molecular markers M. m. musculus-M. m. domesticus, Genet. Res., 2003, vol. 81, pp. 103-114.
44. Ben-Sholomo, R., Neufeld, E., Berger, D., et al., The dynamic of t-haplotype in wild populations of the house mouse Mus musculus domesticus in Israel, Mamm. Genome, 2007, vol. 18, no. 3, pp. 164-172.
45. Safronova, L. D., Petrosyan, V. G., and Orlov, V. N., The expression of transmission ratio distortion (TRD) and the frequency of carriers of t haplotypes in natural populations of house mice Mus musculus, Russ. J. Genet., 2010, vol. 46, no. 5, pp. 578-585.
46. Bruck, D., Male segregation ratio advantage as a factor in maintaining alleles in wild population of house mice, Proc. Natl. Acad. Sci. U. S. A., 1957, vol. 43, no. 1, pp. 152-158.
47. Lenington, S., The t-complex: a story of genes, behaviour and population, Adv. Study Behav., 1989, vol. 20, pp. 51-86.
48. Huang, S. W., Ardlie, K. G., and Yu, H. T., Frequency and distribution of t-haplotypes in the Southeast Asian house mouse (Mus musculus) in Taiwan, Mol. Ecol., 2001, vol. 10, no. 9, pp. 2349-2354.
49. Hiraizumi, Y. and Thomas, A., Suppressor systems of segregation distorter (SD) chromosomes in natural populations of Drosophila melanogaster, Genetics, 1984, vol. 106, pp. 279-292.
50. Manser, A., Lindholm, A. K., Konig, B., and Bagheri, H. C., Polyandry and the decrease of selfish genetic element in wild house mouse population, Evolution, 2011, vol. 65, no. 9, pp. 2435-2447. DOI: 10. 1111/j. 1558-5646. 2011. 01336. x.
51. McDermott, S. R. and Noor, M. A., The role of meiotic drive in hybrid mice sterility, Biol. Sci., 2010, vol. 27, pp. 1272-1285.
52. Charlesworth, B. and Hartl, L. D., Population dynamics of the segregation distortion polymorphism of Drosophila melanogaster, Genetics, 1978, vol. 89, no. 1, pp. 171-192.
53. Hurst, L. D. and Pomiankowski, A., Maintaining Mendelism: might prevention be better than cure?, BioEssays, 1991, vol. 13, no. 6, pp. 305-312.
54. Wu, S. I. and Hammer, M. F., Molecular evolution of ultra-selfish genes of meiotic drive systems, Evolution of Molecular Level, Sealander, R. K. and Clark, A. C., Eds., 1991, pp. 177-203.
55. Wilkinson, G. S. and Fry, C. L., Meiotic drive alters sperm competitive ability in stalk-eyed flies, Proc. R. Soc. London, Ser. B, 2001, vol. 268, pp. 2559-2564.
56. Jaenike, G., Sex ratio meiotic drive in the Drosophila quinaria group, Am. Nat., 1996, vol. 148, pp. 237-254.
57. Frank, S. A., Divergence of meiotic drive suppression systems as an explanation for sex-biased hybrid sterility and inviability, Evolution, 1991, vol. 45, pp. 262-272.
58. Babcock, C. S. and Anderson, W. W., Molecular evolution of the sex-ratio inversion complex in Drosophila pseudoobscura: analysis of the Esterase-5 gene region, Mol. Biol. Evol., 1996, vol. 13, no. 2, pp. 297-306.
59. Wu, C. I. and Beckenbach, A. T., Evidence for extensive genetic differentiation between the sex-ratio and the standard arrangement of Drosophila pseudoobscura and Drosophila persimilis and identification of hybrid sterility factors, Genetics, 1983, vol. 105, pp. 71-86.
60. Lenington, S., Drickamer, L. C., Robinson, A. S., and Erhart, M., Genetic basis for male aggression and survivorship in wild mice (Mus musculus), Genet. Agg. Behav., 1996, vol. 22, pp. 135-145.
61. Drickamer, L. C., Lenington, S., Erhart, M., and Robinson, A. S., Mus domesticus in large outdoor pens: implication for models of t-complex gene frequency, Am. Midl. Nat., 1996, vol. 133, pp. 283-289.
62. Myers, J. H., The absence of t-alleles in feral populations of house mouse, Evolution, 1973, vol. 27, pp. 702-70.
63. Anderson, P. K., Ecological structure and gene flow in small mammals, Symp. Zool. Soc. London, 1970, no. 26, pp. 299-325.
64. Berry, H. J., The population of the house mouse, Sci. Prog., 1977, vol. 64, pp. 341-370.
65. Lenington, S. and Heistler, I. L., Behavior reduction in the transmission of deletions t haplotype by wild house mice, Am. Nat., 1991, vol. 137, pp. 366-378.
66. Lenington, S., Coopersmith, C. B., and Erhart, M., Female preference and variability among t-haplotypes in wild house mice, Am. Nat., 1994, vol. 143, pp. 766-784.
67. Carroll, L. S., Meager, S., Morrison, L., et al., Fitness effects of a selfish gene (the Mus t-complex) are revealed in an ecological context, Evolution, 2004, vol. 58, no. 6, pp. 1318-1328.
68. Dean, M. D., Ardlie, K. G., and Nachman, M. W., The frequency of multiple paternity suggests that sperm competition is common in house mice (Mus domesticus), Mol. Ecol., 2006, vol. 15, pp. 4141-4151.
69. Denn, L., Selection at the gamete level as an evolutionary power: retention of polymorphism for lethals in wild populations of Mus musculus, in Problemy eksperimental'noi biologii (Problems of Experimental Biology), Moscow: Nauka, 1977.
70. Demin, Yu. S. and Safronova, L. D., T locus genetics of house mouse (Mus musculus), Usp. Sovrem. Genet., 1980, no. 9, pp. 97-142.
71. Demin, Yu. S. and Safronova, L. D., Prezygotic selection, Usp. Sovrem. Genet., 1985, no. 13, pp. 202-245.
72. Braden, A. W. H., T-locus in mice: segregation distortion and sterility in the male, The Genetics of the Spermatozoon, (Proc. Int. Sympos.), Edinburgh, 1972, pp. 289-305.
73. Dunn, L., Variation in the transmission ratio of alleles through egg and sperm in Mus musculus, Am. Nat., 1960, vol. 44, pp. 385-393.
74. Dunn, L., Bennett, D., and Cookingham, J., Polymorphisms for lethal alleles in European populations of Mus musculus, J. Mammal., 1973, vol. 54, no. 4, p. 822.
75. Bennett, D., Dunn, L. C., and Artzt, K., Genetic change in mutation at the locus T/t in the mouse, Genetics, 1976, vol. 83, no. 2, pp. 361-372.
76. Snell, G. D., The H-2 locus of the mouse: observations and speculations concerning its comparative genetics and its polymorphism, Folia Biol. (Praha), 1968, vol. 14, no. 5, p. 335-358.
77. Demin, Yu. S. and Safronova, L. D., Cytogenetic influence of female genotype on the intensity of prezygotic selection in mice with t6 and ti 2 haplotypes in T locus, Genetika (Moscow), 1981, vol. 17, no. 4, pp. 637-644.
78. Taylor, D. R. and Ingvarsson, P. K., Common features of segregation distortion in plants and animals, Genetics, 2003, vol. 117, no. 1, pp. 27-35.
79. Cameron, D. R. and Moav, R., Inheritance in Nicotiana tabacum: 27. Pollen killer, an alien genetic locus inducing abortion of microspores not carrying it, Genetics, 1957, vol. 42, pp. 326-335.
80. Buckler, E. S., Phelps-Duer, C. S., Buckler, R. K., et al., Meiotic drive of chromosomal knobs reshaped the maize genome, Genetics, 1999, vol. 153, pp. 415-442.
81. De Vilena, F. P. M. and Sapienza, C., Female meiosis drives karyotypic evolution in mammals, Genetics, 2001, vol. 159, pp. 1179-1189.
82. Orr, H. A. and Irving, S., Segregation distortion in hybrids between the Bogota and USA subspecies of Drosophila pseudoobscura, Genetics, 2005, vol. 169, no. 2, pp. 671-682.
83. Masly, J. P., Jones, C. D., Noor, M. A. F., et al., Gene transposition as a cause of hybrid sterility in Drosophila, Science, 2006, vol. 313, pp. 1448-1450.
84. Presgraves, D. C., Speciation genetics: epistasis, conflict and the origin of species, Curr. Biol., 2007, vol. 17, pp. 125-127.
85. Jaenike, J., Sex chromosome meiotic drive, Ann. Rev. Ecol. Syst., 2001, vol. 22, pp. 25-49.
86. Hurst, L. D., Model for the mechanism of transmission ratio distortion and for t-associated hybrid sterility, Proc. R. Soc. London, Ser. B, 1993, vol. 253, pp. 83-91.
87. Hurst, L. D., Atan, B. O., and Bengtsson, B. O., Genetic conflicts, Q. Rev. Biol., 1996, vol. 71, pp. 317-364.
88. Hurst, G. D. and Werren, G. H., The role of selfish genes elements in eukaryotic evolution, Nat. Rev., 2001, vol. 2, pp. 597-606.
89. Johnston, P. G. and Brown, G. H., A comparison of the relative fitness of genotypes segregating for the tw32 allele in laboratory stock and its possible effect on gene frequency in mouse populations, Am. Nat., 1969, vol. 103, pp. 5-21.
90. Haldane, J. B. S., Sex ratio and unisexual sterility in hybrid animals, J. Genet., 1922, vol. 12, pp. 101-109.
91. Phadnis, N. and Orr, H. A., A single gene causes both male sterility and segregation distortion in Drosophila hybrids, Science, 2009, vol. 323, pp. 376-379.
92. van Boven, M. and Weissing, F. J., Competition at the mouse t-complex: rare are inherently favored, Theor. Popul. Biol., 2001, vol. 60, no. 4, pp. 343-358.
93. Weissing, F. J. and van Boven, M., Selection and segregation distortion in a sex-differentiated population, Theor. Popul. Biol., 2001, vol. 60, no. 4, pp. 327-341.
94. Figueroa, F., Kasahara, M., Tichy, H., et al., Polymorphism of unique noncoding DNA sequences in wild and laboratory mice, Genetics, 1987, vol. 117, pp. 101-108.
95. Figueroa, F., Neufield, E., Ritte, U., and Klein, J., t-Specific DNA polymorphism among wild mice from Israel and Spain, Genetics, 1988, vol. 119, pp. 157-160.
96. Lyon, M. F., Cattanah, D. V., and Charlton, H. M., Genes affecting sex determination in mammals, Mechanisms of Sex Differentiation in Animals and Man, Austin, C. R. and Edwards, R. G., Eds., New York, 1981, pp. 329-386.
97. Temin, R. G., Ganetzky, B., Powers, P. A., et al., Segregation distortion in Drosophila melanogaster: genetic and molecular analyses, Am. Nat., 1991, vol. 137, pp. 287-331.
98. Silver, L. M., Molecular probes define different region of the mouse t-complex, Cell, 1985, vol. 40, pp. 63-69.
99. Wallece, L. T. and Erhart, M. A., Recombination within mouse t-haplotypes has replaced significant segments of specific DNA, Mamm. Genome, 2008, vol. 19, pp. 263-271.
100. Dunn, L. C., Bennett, D., and Cookingam, J., Polymorphisms for lethal alleles in European populations of wild house mice, J. Mammal., 1973, vol. 54, pp. 822-830.
101. Durand, D., Ardlie, K., Buttel, L., et al., Impact of migration and fitness or the stability of lethal t-haplotype polymorphism in Mus musculus a computer study, Genetics, 1997, vol. 145, no. 4, pp. 1093-1108.
102. Levontin, R. C., The Genetic Basis of Evolutionary Change, New York: Columbia Univ. Press, 1974.
103. Demin, Yu. S., Kryukov, V. I., and Orlov, V. N., Analysis of t-haplotypes in natural populations of house mouse: 1. Identification of t-haplotypes in Mus musculus L. populations from Tajikistan, Genetika (Moscow), 1980, vol. 16, no. 7, pp. 1270-1276.
104. Demin, Yu. S and Kryukov, V. I., Analysis of t-haplotypes in natural populations of house mouse: 2. Test for belongings to complementation group tw73, Genetika (Moscow), 1983, vol. 19, no. 11, pp. 1840-1843.
105. Demin, Yu. S. and Mazin, S. M., Detection and analysis of t-haplotypes in the urban population of house mouse, Mus musculus, Dokl. Akad. Nauk. SSSR, 1984, vol. 277, no. 6, pp. 1476-1478.
106. Demin, Yu. S., Mazin, S. M., and Safronova, L. D., Results of analysis of the t-haplotypes isolated from the gene pool in Moscow populations of house mouse, Dokl. Akad. Nauk SSSR, 1986, vol. 285, no. 3, pp. 507-510.
107. Luis-Miguel Chevin, L.-M. and Hospital, F., The hitchhiking effect of an autosomal meiotic drive gene, Genetics, 2006, vol. 173, no. 3, pp. 1829-1832.
108. Chubykin, V. L., The nature of mildly deleterious mutations eliminated upon sexual reproduction in meiosis, Adv. Life Sci., 2012, vol. 2, no. 6, pp. 156-169.