Skip to main content
PMC home page
Genetics logoLink to Genetics
. 1996 Dec;144(4):1787–1797. doi: 10.1093/genetics/144.4.1787

Low Frequency of Mouse T Haplotypes in Wild Populations Is Not Explained by Modifiers of Meiotic Drive

K G Ardlie 1, L M Silver 1
PMCID: PMC1207728  PMID: 8978064

Abstract

t haplotypes are naturally occurring forms of mouse chromosome 17 that show non-Mendelian transmission from heterozygous +/t males. In laboratory studies, transmission ratios of >=0.90 or higher are typically observed. With transmission ratios of this level, theoretical analyses predict high frequencies of t haplotypes (~ 75%) in wild populations. In contrast, empirical frequencies of only 15-25% are typically found. This has led to the suggestion that modifiers of drive may play a role in reducing t frequencies. We have measured transmission ratio distortion (TRD) levels in wild +/t mice to examine this hypothesis. TRD was very high in both litters collected from wild-caught pregnant females, and in wild litters bred in the laboratory (mean = 0.9). Contrary to the results of other studies, we found no difference in TRD levels between semilethal and lethal t haplotypes nor between litters conceived from cycling or postpartum estrus. We found three litters with aberrantly low TRDs that were all multiply sired, although the role this might play in natural populations is unknown. These findings show a general absence of modifiers of drive in natural populations and suggest that other factors are responsible for the low observed frequencies of wild t haplotypes.

Full Text

The Full Text of this article is available as a PDF (3.0 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. ANDERSON P. K. LETHAL ALLELES IN MUS MUSCULUS: LOCAL DISTRIBUTION AND EVIDENCE FOR ISOLATION OF DEMES. Science. 1964 Jul 10;145(3628):177–178. doi: 10.1126/science.145.3628.177. [DOI] [PubMed] [Google Scholar]
  2. Ardlie K. G., Silver L. M. Recent evolution of mouse t haplotypes at polymorphic microsatellites associated with the t complex responder (Tcr) locus. Genet Res. 1996 Feb;67(1):1–10. doi: 10.1017/s0016672300033425. [DOI] [PubMed] [Google Scholar]
  3. Artzt K. Gene mapping within the T/t complex of the mouse. III: t-Lethal genes are arranged in three clusters on chromosome 17. Cell. 1984 Dec;39(3 Pt 2):565–572. doi: 10.1016/0092-8674(84)90463-x. [DOI] [PubMed] [Google Scholar]
  4. Artzt K., Shin H. S., Bennett D. Gene mapping within the T/t complex of the mouse. II. Anomalous position of the H-2 complex in t haplotypes. Cell. 1982 Mar;28(3):471–476. doi: 10.1016/0092-8674(82)90201-x. [DOI] [PubMed] [Google Scholar]
  5. BRADEN A. W. Influence of time of mating on the segregation ratio of alleles at the T locus in the house mouse. Nature. 1958 Mar 15;181(4611):786–787. doi: 10.1038/181786a0. [DOI] [PubMed] [Google Scholar]
  6. Bennett D., Alton A. K., Artzt K. Genetic analysis of transmission ratio distortion by t-haplotypes in the mouse. Genet Res. 1983 Feb;41(1):29–45. doi: 10.1017/s0016672300021042. [DOI] [PubMed] [Google Scholar]
  7. Brown J., Cebra-Thomas J. A., Bleil J. D., Wassarman P. M., Silver L. M. A premature acrosome reaction is programmed by mouse t haplotypes during sperm differentiation and could play a role in transmission ratio distortion. Development. 1989 Aug;106(4):769–773. doi: 10.1242/dev.106.4.769. [DOI] [PubMed] [Google Scholar]
  8. Bruck D. MALE SEGREGATION RATIO ADVANTAGE AS A FACTOR IN MAINTAINING LETHAL ALLELES IN WILD POPULATIONS OF HOUSE MICE. Proc Natl Acad Sci U S A. 1957 Jan 15;43(1):152–158. doi: 10.1073/pnas.43.1.152. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Church G. M., Gilbert W. Genomic sequencing. Proc Natl Acad Sci U S A. 1984 Apr;81(7):1991–1995. doi: 10.1073/pnas.81.7.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Curtsinger J. W., Feldman M. W. Experimental and Theoretical Analysis of the "Sex-Ratio" Polymorphism in DROSOPHILA PSEUDOOBSCURA. Genetics. 1980 Feb;94(2):445–466. doi: 10.1093/genetics/94.2.445. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Delarbre C., Kashi Y., Boursot P., Beckmann J. S., Kourilsky P., Bonhomme F., Gachelin G. Phylogenetic distribution in the genus Mus of t-complex-specific DNA and protein markers: inferences on the origin of t-haplotypes. Mol Biol Evol. 1988 Mar;5(2):120–133. doi: 10.1093/oxfordjournals.molbev.a040481. [DOI] [PubMed] [Google Scholar]
  12. Dunn L C. Studies of the Genetic Variability in Populations of Wild House Mice. II. Analysis of Eight Additional Alleles at Locus T. Genetics. 1957 May;42(3):299–311. doi: 10.1093/genetics/42.3.299. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Dunn L C, Suckling J. Studies of the Genetic Variability in Wild Populations of House Mice. I. Analysis of Seven Alleles at Locus T. Genetics. 1956 May;41(3):344–352. doi: 10.1093/genetics/41.3.344. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Erickson R. P. Haploid gene expresion versus meiotic drive: the relevance of intercellular bridges during spermatogenesis. Nat New Biol. 1973 Jun 13;243(128):210–212. doi: 10.1038/newbio243210a0. [DOI] [PubMed] [Google Scholar]
  15. Feinberg A. P., Vogelstein B. "A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity". Addendum. Anal Biochem. 1984 Feb;137(1):266–267. doi: 10.1016/0003-2697(84)90381-6. [DOI] [PubMed] [Google Scholar]
  16. Fox H. S., Martin G. R., Lyon M. F., Herrmann B., Frischauf A. M., Lehrach H., Silver L. M. Molecular probes define different regions of the mouse t complex. Cell. 1985 Jan;40(1):63–69. doi: 10.1016/0092-8674(85)90309-5. [DOI] [PubMed] [Google Scholar]
  17. Garside W., Hillman N. The transmission ratio distortion of the th2-haplotype in vivo and in vitro. Genet Res. 1989 Feb;53(1):25–28. doi: 10.1017/s001667230002783x. [DOI] [PubMed] [Google Scholar]
  18. Garside W., Ruangvoravat C., Dolan P., Hillman N. The in vivo and in vitro transmission ratio distortion of one complete and two partial t haplotypes in mice. Genet Res. 1991 Apr;57(2):153–157. doi: 10.1017/s0016672300029232. [DOI] [PubMed] [Google Scholar]
  19. Gummere G. R., McCormick P. J., Bennett D. The influence of genetic background and the homologous chromosome 17 on t-haplotype transmission ratio distortion in mice. Genetics. 1986 Sep;114(1):235–245. doi: 10.1093/genetics/114.1.235. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Hammer M. F., Schimenti J., Silver L. M. Evolution of mouse chromosome 17 and the origin of inversions associated with t haplotypes. Proc Natl Acad Sci U S A. 1989 May;86(9):3261–3265. doi: 10.1073/pnas.86.9.3261. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Hammer M. F., Silver L. M. Phylogenetic analysis of the alpha-globin pseudogene-4 (Hba-ps4) locus in the house mouse species complex reveals a stepwise evolution of t haplotypes. Mol Biol Evol. 1993 Sep;10(5):971–1001. doi: 10.1093/oxfordjournals.molbev.a040051. [DOI] [PubMed] [Google Scholar]
  22. Herrmann B., Bućan M., Mains P. E., Frischauf A. M., Silver L. M., Lehrach H. Genetic analysis of the proximal portion of the mouse t complex: evidence for a second inversion within t haplotypes. Cell. 1986 Feb 14;44(3):469–476. doi: 10.1016/0092-8674(86)90468-x. [DOI] [PubMed] [Google Scholar]
  23. Hiraizumi Y., Albracht J. M., Albracht B. C. X-linked elements associated with negative segregation distortion in the SD system of Drosophila melanogaster. Genetics. 1994 Sep;138(1):145–152. doi: 10.1093/genetics/138.1.145. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Johnson L. R., Pilder S. H., Bailey J. L., Olds-Clarke P. Sperm from mice carrying one or two t haplotypes are deficient in investment and oocyte penetration. Dev Biol. 1995 Mar;168(1):138–149. doi: 10.1006/dbio.1995.1067. [DOI] [PubMed] [Google Scholar]
  25. Lewontin R C, Dunn L C. The Evolutionary Dynamics of a Polymorphism in the House Mouse. Genetics. 1960 Jun;45(6):705–722. doi: 10.1093/genetics/45.6.705. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Lyon M. F. Male sterility of the mouse t-complex is due to homozygosity of the distorter genes. Cell. 1986 Jan 31;44(2):357–363. doi: 10.1016/0092-8674(86)90770-1. [DOI] [PubMed] [Google Scholar]
  27. McGrath J., Hillman N. The in vitro transmission frequency of the t6 allele. Nature. 1980 Jan 31;283(5746):479–481. doi: 10.1038/283479a0. [DOI] [PubMed] [Google Scholar]
  28. Olds-Clarke P., Peitz B. Fertility of sperm from t/+ mice: evidence that +-bearing sperm are dysfunctional. Genet Res. 1986 Feb;47(1):49–52. doi: 10.1017/s0016672300024502. [DOI] [PubMed] [Google Scholar]
  29. Prout T., Bundgaard J., Bryant S. Population genetics of modifiers of meiotic drive. I. The solution of a special case and some general implications. Theor Popul Biol. 1973 Dec;4(4):446–465. doi: 10.1016/0040-5809(73)90020-8. [DOI] [PubMed] [Google Scholar]
  30. Ruvinsky A., Polyakov A., Agulnik A., Tichy H., Figueroa F., Klein J. Low diversity of t haplotypes in the eastern form of the house mouse, Mus musculus L. Genetics. 1991 Jan;127(1):161–168. doi: 10.1093/genetics/127.1.161. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Röhme D., Fox H., Herrmann B., Frischauf A. M., Edström J. E., Mains P., Silver L. M., Lehrach H. Molecular clones of the mouse t complex derived from microdissected metaphase chromosomes. Cell. 1984 Mar;36(3):783–788. doi: 10.1016/0092-8674(84)90358-1. [DOI] [PubMed] [Google Scholar]
  32. Sarvetnick N., Fox H. S., Mann E., Mains P. E., Elliott R. W., Silver L. M. Nonhomologous pairing in mice heterozygous for a t haplotype can produce recombinant chromosomes with duplications and deletions. Genetics. 1986 Jul;113(3):723–734. doi: 10.1093/genetics/113.3.723. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Schimenti J., Vold L., Socolow D., Silver L. M. An unstable family of large DNA elements in the center of the mouse t complex. J Mol Biol. 1987 Apr 20;194(4):583–594. doi: 10.1016/0022-2836(87)90235-x. [DOI] [PubMed] [Google Scholar]
  34. Seitz A. W., Bennett D. Transmission distortion of t-haplotypes is due to interactions between meiotic partners. Nature. 1985 Jan 10;313(5998):143–144. doi: 10.1038/313143a0. [DOI] [PubMed] [Google Scholar]
  35. Silver L. M. Mouse t haplotypes. Annu Rev Genet. 1985;19:179–208. doi: 10.1146/annurev.ge.19.120185.001143. [DOI] [PubMed] [Google Scholar]
  36. Silver L. M. The peculiar journey of a selfish chromosome: mouse t haplotypes and meiotic drive. Trends Genet. 1993 Jul;9(7):250–254. doi: 10.1016/0168-9525(93)90090-5. [DOI] [PubMed] [Google Scholar]
  37. Willison K. R., Dudley K., Potter J. Molecular cloning and sequence analysis of a haploid expressed gene encoding t complex polypeptide 1. Cell. 1986 Mar 14;44(5):727–738. doi: 10.1016/0092-8674(86)90839-1. [DOI] [PubMed] [Google Scholar]
  38. Wu C. I., True J. R., Johnson N. Fitness reduction associated with the deletion of a satellite DNA array. Nature. 1989 Sep 21;341(6239):248–251. doi: 10.1038/341248a0. [DOI] [PubMed] [Google Scholar]
  39. Wu C. I. Virility Deficiency and the Sex-Ratio Trait in DROSOPHILA PSEUDOOBSCURA. I. Sperm Displacement and Sexual Selection. Genetics. 1983 Nov;105(3):651–662. doi: 10.1093/genetics/105.3.651. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Wu C. I. Virility Deficiency and the Sex-Ratio Trait in DROSOPHILA PSEUDOOBSCURA. II. Multiple Mating and Overall Virility Selection. Genetics. 1983 Nov;105(3):663–679. doi: 10.1093/genetics/105.3.663. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. YANAGISAWA K., DUNN L. C., BENNETT D. On the mechanism of abnormal transmission ratios at T locus in the house mouse. Genetics. 1961 Dec;46:1635–1644. doi: 10.1093/genetics/46.12.1635. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES