Skip to main content
NCBI home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1992 Aug 1;89(15):6851–6855. doi: 10.1073/pnas.89.15.6851

Evolution of the mouse t haplotype: recent and worldwide introgression to Mus musculus.

T Morita 1, H Kubota 1, K Murata 1, M Nozaki 1, C Delarbre 1, K Willison 1, Y Satta 1, M Sakaizumi 1, N Takahata 1, G Gachelin 1, et al.
PMCID: PMC49602  PMID: 1495973

Abstract

Mouse t haplotypes are variants of chromosome 17, consisting of four inversions. Despite the homozygous lethality and pleiotropic effect on embryonic development, sperm production, and recombination, they have widely spread in natural populations of the house mouse (10-40% in frequency) because of the meiotic drive advantage. We sequenced 14 Tcp-1 (t-complex polypeptide 1) genes from four t haplotypes, nine wild mice, and a rat as a reference. From a comparison of intron sequences of 610 base pairs, we dated the origin of t haplotypes to 2.9 +/- 0.7 million years ago, which predates the splitting of Mus musculus subspecies (approximately 1 million years ago). However, the Tcp-1 intron sequences of t haplotypes from different M. musculus subspecies from various parts of the world show no divergence, indicating the recent introgression (no earlier than 0.8 million years ago) of a single ancestral type. Nucleotide changes in coding regions are also consistent with this conclusion. Hence, polymorphisms among t haplotypes including lethality factors have accumulated during this short time period independently in each M. musculus subspecies.

Full text

PDF
6851

Selected References

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

  1. Bonhomme F., Catalan J., Britton-Davidian J., Chapman V. M., Moriwaki K., Nevo E., Thaler L. Biochemical diversity and evolution in the genus Mus. Biochem Genet. 1984 Apr;22(3-4):275–303. doi: 10.1007/BF00484229. [DOI] [PubMed] [Google Scholar]
  2. Bonhomme F. Evolutionary relationships in the genus Mus. Curr Top Microbiol Immunol. 1986;127:19–34. doi: 10.1007/978-3-642-71304-0_3. [DOI] [PubMed] [Google Scholar]
  3. Bullard D. C., Schimenti J. C. Molecular cloning and genetic mapping of the t complex responder candidate gene family. Genetics. 1990 Apr;124(4):957–966. doi: 10.1093/genetics/124.4.957. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. 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]
  5. Erhart M. A., Phillips S. J., Nadeau J. H. Contrasting patterns of evolution in the proximal and distal regions of the mouse t complex. Curr Top Microbiol Immunol. 1988;137:70–76. doi: 10.1007/978-3-642-50059-6_11. [DOI] [PubMed] [Google Scholar]
  6. Ferris S. D., Sage R. D., Prager E. M., Ritte U., Wilson A. C. Mitochondrial DNA evolution in mice. Genetics. 1983 Nov;105(3):681–721. doi: 10.1093/genetics/105.3.681. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Gupta R. S. Sequence and structural homology between a mouse T-complex protein TCP-1 and the 'chaperonin' family of bacterial (GroEL, 60-65 kDa heat shock antigen) and eukaryotic proteins. Biochem Int. 1990;20(4):833–841. [PubMed] [Google Scholar]
  8. 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]
  9. Klein J., Golubić M., Budimir O., Schöpfer R., Kasahara M., Figueroa F. On the origin of t chromosomes. Curr Top Microbiol Immunol. 1986;127:239–246. doi: 10.1007/978-3-642-71304-0_27. [DOI] [PubMed] [Google Scholar]
  10. Krayev A. S., Kramerov D. A., Skryabin K. G., Ryskov A. P., Bayev A. A., Georgiev G. P. The nucleotide sequence of the ubiquitous repetitive DNA sequence B1 complementary to the most abundant class of mouse fold-back RNA. Nucleic Acids Res. 1980 Mar 25;8(6):1201–1215. doi: 10.1093/nar/8.6.1201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Kubota H., Morita T., Nagata T., Takemoto Y., Nozaki M., Gachelin G., Matsushiro A. Nucleotide sequence of mouse Tcp-1a cDNA. Gene. 1991 Sep 15;105(2):269–273. doi: 10.1016/0378-1119(91)90162-5. [DOI] [PubMed] [Google Scholar]
  12. Kubota H., Morita T., Satta Y., Nozaki M., Matsushiro A. Nucleotide sequence of a mouse Tcp-1 pseudogene: a nucleotide record for a t complex gene carried by an ancestor of the mouse. Mamm Genome. 1992;2(4):246–251. doi: 10.1007/BF00355434. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. Lyon M. F. Transmission ratio distortion in mouse t-haplotypes is due to multiple distorter genes acting on a responder locus. Cell. 1984 Jun;37(2):621–628. doi: 10.1016/0092-8674(84)90393-3. [DOI] [PubMed] [Google Scholar]
  15. Maps of mouse chromosome 17: first report. Committee for Mouse Chromosome 17. Mamm Genome. 1991;1(1):5–29. [PubMed] [Google Scholar]
  16. Miyata T., Hayashida H., Kikuno R., Hasegawa M., Kobayashi M., Koike K. Molecular clock of silent substitution: at least six-fold preponderance of silent changes in mitochondrial genes over those in nuclear genes. J Mol Evol. 1982;19(1):28–35. doi: 10.1007/BF02100221. [DOI] [PubMed] [Google Scholar]
  17. Moriwaki K., Miyashita N., Suzuki H., Kurihara Y., Yonekawa H. Genetic features of major geographical isolates of Mus musculus. Curr Top Microbiol Immunol. 1986;127:55–61. doi: 10.1007/978-3-642-71304-0_6. [DOI] [PubMed] [Google Scholar]
  18. Nizetić D., Figueroa F., Klein J. Evolutionary relationships between the t and H-2 haplotypes in the house mouse. Immunogenetics. 1984;19(4):311–320. doi: 10.1007/BF00345404. [DOI] [PubMed] [Google Scholar]
  19. 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]
  20. Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987 Jul;4(4):406–425. doi: 10.1093/oxfordjournals.molbev.a040454. [DOI] [PubMed] [Google Scholar]
  21. Silver L. M., Artzt K., Bennett D. A major testicular cell protein specified by a mouse T/t complex gene. Cell. 1979 Jun;17(2):275–284. doi: 10.1016/0092-8674(79)90153-3. [DOI] [PubMed] [Google Scholar]
  22. Silver L. M., Hammer M., Fox H., Garrels J., Bucan M., Herrmann B., Frischauf A. M., Lehrach H., Winking H., Figueroa F. Molecular evidence for the rapid propagation of mouse t haplotypes from a single, recent, ancestral chromosome. Mol Biol Evol. 1987 Sep;4(5):473–482. doi: 10.1093/oxfordjournals.molbev.a040457. [DOI] [PubMed] [Google Scholar]
  23. 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]
  24. Sokal R. R., Oden N. L., Wilson C. Genetic evidence for the spread of agriculture in Europe by demic diffusion. Nature. 1991 May 9;351(6322):143–145. doi: 10.1038/351143a0. [DOI] [PubMed] [Google Scholar]
  25. Ursic D., Culbertson M. R. The yeast homolog to mouse Tcp-1 affects microtubule-mediated processes. Mol Cell Biol. 1991 May;11(5):2629–2640. doi: 10.1128/mcb.11.5.2629. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. 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]
  27. Wilson A. C., Carlson S. S., White T. J. Biochemical evolution. Annu Rev Biochem. 1977;46:573–639. doi: 10.1146/annurev.bi.46.070177.003041. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES