Hostname: page-component-8448b6f56d-jr42d Total loading time: 0 Render date: 2024-04-19T10:55:28.145Z Has data issue: false hasContentIssue false

Recent evolution of mouse t haplotypes at polymorphic microsatellites associated with the t complex responder (Tcr) locus

Published online by Cambridge University Press:  14 April 2009

Kristin G. Ardlie
Affiliation:
Department of Ecology and Evolutionary Biology and the Department of Molecular Biology, Princeton University, Princeton, NJ 08544
Lee M. Silver
Affiliation:
Department of Ecology and Evolutionary Biology and the Department of Molecular Biology, Princeton University, Princeton, NJ 08544
Rights & Permissions [Opens in a new window]

Summary

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Microsatellites closely associated with each member of the Tcp1O gene family were amplified simultaneously from t haplotype and wild-type forms of mouse chromosome 17, by PCR. The t complex responder (Tcr) locus, which plays a central role in transmission ratio distortion, maps within the Tcp10 cluster on the t haplotype. Thus the amplified set of microsatellite loci (referred to collectively as Tcp10ms) provides a direct marker for this central component of the meiotic drive system associated with all naturally occurring t haplotypes. A unique Tcp10ms pattern of microsatellite alleles was obtained for a number of independent, laboratory-maintained complete and partial t haplotypes. Independent t chromosomes found in wild mice from US populations also had unique patterns, even when they were classified within the same lethal complementation group. Wild and laboratory chromosomes in the tw5 group showed similarly-sized but non-identical Tcp10ms patterns, suggesting they share a recent common ancestor. These chromosomes are likely to have derived from an ancestral chromosome within the founding population of North American house mice. The Tcp10ms pattern was also shown to be useful in field studies for distinguishing among independentt haplotypes, when more than one is present within a single population.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1996

References

Artz, K., Shin, H. S., Bennett, D., & Dimeo-Talento, A., (1985). Analysis of major histocompatability complex haplotypes of t-chromosomes reveals that the majority of diversity is generated by recombination. Journal of Experimental Medicine 162, 93104.CrossRefGoogle Scholar
Beckman, J. S., & Weber, J. L., (1992). Survey of human and rat microsatellites. Genomics 12, 627631.CrossRefGoogle ScholarPubMed
Bennett, D., (1975). The T-locus of the mouse. Cell 6, 441–154.CrossRefGoogle Scholar
Bruford, M. W., & Wayne, R. K., (1993). Microsatellites and their application to population genetic studies. Current Opinions in Genetics and Development 3, 939943.CrossRefGoogle ScholarPubMed
Bullard, D. C., & Schimenti, J. C., (1990). Molecular cloning and genetic mapping of the t complex responder candidate gene family. Genetics 124, 957966.CrossRefGoogle Scholar
Bullard, D. C., & Schimenti, J. C., (1991). Molecular structure of Tcp-10 genes from the t complex responder locus. Mammalian Genome 1, 228234.CrossRefGoogle ScholarPubMed
Bullard, D. C., Ticknor, C., & Schimenti, J. C., (1992). Functional analysis of a t complex responder locus transgene. Mammalian Genome 3, 588596.CrossRefGoogle ScholarPubMed
Callen, D. F., Thompson, A. D., Shen, Y., Phillips, H. A., Richards, R. I., Mulley, J. C., & Sutherland, G. R., (1993). Incidence and origin of ‘null’ alleles in the (AC)n microsatellite markers. American Journal of Human Genetics 52, 922927.Google Scholar
Cebra-Thomas, J. A., Decker, C, Snyder, L. C, Pilder, S. H., & Silver, L. M., (1991). Allele- and haploid-specific product generated by alternative splicing from a mouse t complex responder locus candidate. Nature 349, 239241.CrossRefGoogle Scholar
Committee for Mouse Chromosome 17 (1991). Maps of mouse chromosome 17: First report. Mammalian Genome 1, 529.CrossRefGoogle Scholar
Davies, P. O., & Willison, K. R., (1991). Sequence of the t-complex Tcp-10at gene and examination of the Tcp-10at gene family. Mammalian Genome 1, 235241.CrossRefGoogle ScholarPubMed
Dietrich, W., Katz, H., Lincoln, S., Shin, H.-S., Friedman, J., Dracopoli, N. C., & Lander, E., (1992). A genetic map of the mouse suitable for typing intraspecific crosses. Genetics 131, 423447.CrossRefGoogle ScholarPubMed
Dunn, L. C., (1957). Evidence of evolutionary forces leading to the spread of lethal genes in wild populations of house mice. Proceedings of the National Academy of Sciences, USA 43, 158163.CrossRefGoogle Scholar
Ebersole, T., Lai, F., & Artzt, K., (1992). New molecular markers for the distal end of the t-complex and their relationships to mutations affecting mouse development. Genetics 131, 175182.CrossRefGoogle ScholarPubMed
Ellegren, H., (1995). Mutation rates at porcine microsatellite loci. Mammalian Genome 6, 376377.CrossRefGoogle ScholarPubMed
Figueroa, F., Neufeld, E., Ritte, U., & Klein, J., (1988). t-specific DNA polymorphisms among wild mice from Israel and Spain. Genetics 119, 157–60.CrossRefGoogle ScholarPubMed
Fox, H. S., Martin, G. R., Lyon, M. F., Herrmann, B., Frischauf, A.-M., Lehrach, H., & Silver, L. M., (1985). Molecular probes define different regions of the mouse t complex. Cell 40, 6369.CrossRefGoogle ScholarPubMed
Hamada, H., Petrino, M. G., & Kakunaga, T., (1982). A novel repeated element with Z-DNA-forming potential is widely found in evolutionarily diverse eukaryotic genomes. Proceedings of the National Academy of Sciences, USA 79, 64656469.CrossRefGoogle ScholarPubMed
Hammer, M. F., Schimenti, J., & Silver, L, M., (1989). Evolution of mouse chromosome 17 and the origin of inversions association with t haplotypes. Proceedings of the National Academy of Sciences, USA 86, 32613265.CrossRefGoogle ScholarPubMed
Hammer, M. F., & Silver, L. M., (1993). Phylogenetic analysis of the alpha-globin pseudogene-4 (Hba-ps4) locus in the house mouse species complex reveals a stepwise evolution of t haplotypes. Molecular Biology and Evolution 10, 9711001.Google ScholarPubMed
Herrmann, B., Búcan, M., Mains, P. E., Frischauf, A.-M., Silver, L. M., & Lehrach, H., (1986). Genetic analysis of the proximal portion of the mouse t complex: evidence for a second inversion within t haplotypes. Cell 44, 469476.CrossRefGoogle Scholar
Herrmann, B. G., Barlow, D. P., & Lehrach, H., (1987). A large inverted duplication allows homologous recombination between chromosomes heterozygous for the proximal t complex inversion. Cell 48, 813825.CrossRefGoogle ScholarPubMed
Higuchi, R. G., & Ochman, H., (1989). Production of single-stranded DNA templates by exonuclease digestion following the polymerase chain reaction. Nucleic Acids Research 17, 5865.CrossRefGoogle ScholarPubMed
Hino, O., Testa, J. R., Buetow, K. H., Taguchi, T., Zhou, J.-Y., Bremer, M., Bruzel, A., Yeung, R., Levan, G., Levan, K. K., Knudson, A. G., & Tartof, K. D., (1993). Universal mapping probes and the origin of human chromosome 3. Proceedings of the National Academy of Sciences, USA 90, 730734.CrossRefGoogle ScholarPubMed
Hogan, B., Beddington, R., Costantini, F., & Lacy, E., (1994). Manipulating the Mouse Embryo: A Laboratory Manual, Second Edition. Cold Spring Harbor Laboratory Press, Cold Spring Harbor.Google Scholar
Horiuchi, Y., Agulnik, A., Figueroa, F., Tichy, H., & Klein, J., (1992). Polymorphisms distinguishing different mouse species and t haplotypes. Genetical Research 60, 4352.CrossRefGoogle ScholarPubMed
Howard, C. A., Gummere, G. R., Lyon, M. F., Bennett, D., & Artzt, K., (1990). Genetic Molecular analysis of the proximal region of the mouse t-complex using new molecular probes and partial t-haplotypes. Genetics 126, 11031114.CrossRefGoogle ScholarPubMed
Hughes, C. R., & Queller, D. C., (1993). Detection of highly polymorphic microsatellite loci in a species with little allozyme polymorphism. Molecular Ecology 2, 131137.CrossRefGoogle Scholar
Islam, S. D., Pilder, S. H., Decker, C. L., Cebra-Thomas, J. A., & Silver, L. M., (1993). The human homolog of a candidate mouse t complex responder gene: conserved motifs and evolution with punctuated equilibria. Human Molecular Genetics 2, 20752079.CrossRefGoogle Scholar
Klein, J., Sipos, P., & Figueroa, F., (1984). Polymorphism of t-complex genes in European wild mice. Genetical Research 44, 3946.CrossRefGoogle Scholar
Kreitman, M., & Landweber, L. F., (1989). A strategy for producing single stranded DNA in the polymerase chain reaction: a direct method for genomic sequencing. Gene Analysis Techniques 6, 8488.CrossRefGoogle ScholarPubMed
Lai, F., & Artzt, K., (1992). Map positions of four dinucleotide repeats in the mouse t complex. Mammalian Genome 3, 476477.CrossRefGoogle ScholarPubMed
Lenington, S., Franks, P., & Williams, J., (1988). Distribution of t haplotypes in natural populations of wild house mice. Journal of Mammalogy 69, 489499.CrossRefGoogle Scholar
Litt, M., & Lucy, J. A., (1989). A hypervariable microsatellite revealed by in vitro amplification of a dinucleotide repeat within the cardiac muscle actin gene. American Journal of Human Genetics 44, 397401.Google ScholarPubMed
Love, J. M., Knight, A. M., McAleer, M. A., & Todd, J. A., (1990). Towards construction of a high resolution map of the mouse genome using PCR-analyzed microsatellites. Nucleic Acids Research 18, 41234130.CrossRefGoogle Scholar
Lundrigan, B. L., & Tucker, P. K., (1994). Tracing paternal ancestry in mice, using the Y-linked, sex-determining locus. Sry. Molecular Biology and Evolution 11, 483492.Google ScholarPubMed
Lyon, M. F., (1984). Transmission ratio distortion in mouse t-haplotypes is due to multiple distorter genes acting on a responder locus. Cell 37, 621628.CrossRefGoogle ScholarPubMed
Lyon, M. F., (1986). Male sterility of the mouse t-complex is due to homozygosity of the distorter genes. Cell 44, 357363.CrossRefGoogle ScholarPubMed
Lyon, M. F., & Zenthon, J., (1987). Differences in or near the responder region of complete and partial mouse t-haplotypes. Genetical Research 50, 2934.CrossRefGoogle ScholarPubMed
Moore, S. S., Sargeant, L. L., King, T. J., Mattick, J. S., Georges, M., & Hetzel, D. J. S., (1991). The conservation of dinucleotide microsatellites among mammalian genomes allows the use of heterologous PCR primer pairs in closely related species. Genomics 10, 654660.CrossRefGoogle ScholarPubMed
Morita, T., Kubota, H., Murata, K., Nozaki, M., Delarbre, C, Willison, K., Satta, Y., Sakaizumi, M., Takahata, N., Gachelin, G., & Matsushiro, A., (1992). Evolution of the mouse t haplotype: Recent and worldwide introgression to Mus musculus. Proceedings of the National Academy of Sciences, USA 89, 68516855.CrossRefGoogle ScholarPubMed
Pemberton, J. M., Slate, J., Bancroft, D. R., & Barrett, J. A., (1995). Nonamplifying alleles at microsatellite loci: a caution for parentage and population studies. Molecular Ecology 4, 249252.CrossRefGoogle ScholarPubMed
Petras, M. L., (1967). Studies of natural populations of Mus. II. Polymorphism at the t locus. Evolution 21, 466478.CrossRefGoogle ScholarPubMed
Pilder, S. H., Decker, C. L., Islam, S., Buck, C, Cebra-Thomas, J. A., & Silver, L. M., (1992). Concerted evolution of the mouse Tcp-10 gene family: implications for the functional basis of t haplotype transmission ratio distortion. Genomics 12, 3541.CrossRefGoogle ScholarPubMed
Rosen, L. L., Bullard, D. C., Silver, L. M., & Schimenti, J. C., (1990). Molecular cloning of the t complex responder genetic locus. Genomics 8, 134140.CrossRefGoogle Scholar
Schimenti, J., Cebra-Thomas, J. A., Decker, C, Islam, S., Pilder, S. H., & Silver, L. M., (1988). A candidate gene family for the mouse t complex responder (Tcr) locus responsible for haploid effects on sperm function. Cell 55, 7178.CrossRefGoogle Scholar
Schimenti, J., Vold, L., Socolow, D., & Silver, L. M., (1987). An unstable family of large DNA elements in the center of the mouse t complex. Journal of Molecular Biology 194, 583594.CrossRefGoogle Scholar
Schlötterer, C., & Tautz, D., (1992). Slippage synthesis of simple sequence DNA. Nucleic Acids Research 20, 211215.CrossRefGoogle ScholarPubMed
Silver, L. M., (1983). Reevaluation of the evidence for the generation of new lethal t haplotypes by mutation. Immunogenetics 18, 9196.CrossRefGoogle ScholarPubMed
Silver, L. M., (1985). Mouse t haplotypes. Annual Reviews of Genetics 19, 179208.CrossRefGoogle ScholarPubMed
Silver, L. M., (1993). The peculiar journey of a selfish chromosome: mouse t haplotypes and meiotic drive. Trends in Genetics 9, 250254.CrossRefGoogle ScholarPubMed
Silver, L. M., (1995). Mouse Genetics: Concepts and Applications, Oxford University Press, New York.Google Scholar
Silver, L. M., Hammer, M., Fox, H., Garrels, J., Búcan, M., Herrmann, B., Frischauf, A. M., Lehrach, H., Winking, H., Figueroa, F., & Klein, J., (1987). Molecular evidence for the rapid propagation of mouse t haplotypes from a single, recent, ancestral chromosome. Molecular Biology and Evolution 4, 473482.Google ScholarPubMed
Silver, L. M., & Remis, D., (1987). Five of the nine genetically defined regions of mouse t haplotypes are involved in transmission ratio distortion. Genetical Research 49, 5156.CrossRefGoogle ScholarPubMed
Silver, L. M., Uman, J., Danska, J., & Garrels, J. I., (1983). A diversified set of testicular cell proteins specified by genes within the mouse t complex. Cell 35, 3545.CrossRefGoogle ScholarPubMed
Slatkin, M., (1995). A measure of population subdivision based on microsatellite allele frequencies. Genetics 139, 457462.CrossRefGoogle ScholarPubMed
Stallings, R. L., (1994). Distribution of trinucleotide microsatellites in different categories of mammalian genomic sequences: Implications for human genetic diseases. Genomics 21, 116121.CrossRefGoogle ScholarPubMed
Stallings, R. L., (1995). Conservation and evolution of (CT)n/(GA)n microsatellite sequences at orthologous positions in diverse mammalian genomes. Genomics 25, 107113.CrossRefGoogle Scholar
Stallings, R. L., Ford, A. F., Nelson, D., Torney, D. C., Hildebrand, C. E., & Moyzis, R. K., (1991). Evolution and distribution of (GT)n repetitive sequences in mammalian genomes. Genomics 10, 807815.CrossRefGoogle ScholarPubMed
Stephan, W., & Cho, S., (1994). Possible role of natural selection in the formation of tandem-repetitive noncoding DNA. Genetics 136, 333341.CrossRefGoogle ScholarPubMed
Tautz, D., (1993). Notes on the defunction and nomenclature of tandemly repetitive DNA sequences. In DNA Fingerprinting: State of the science, (ed. Pena, S. D. J., Chakraborty, R., Epplen, J. T. and Jeffreys, A. J.) pp. 21–28, Basel: Birkhauser Verlag.Google Scholar
Tautz, D., & Renz, M., (1984). Simple sequences are ubiquitous repetitive components of eukaryotic genomes. Nucleic Acids Research 12, 41274138.CrossRefGoogle ScholarPubMed
Uehara, H., Ebersole, T., Bennett, D., & Artzt, K., (1990). Submegabase clusters of unstable tandem repeats unique to the Tla region of mouse t haplotypes. Genetics 126, 10931102.CrossRefGoogle Scholar
Valdes, A. M., Slatkin, M., & Freimer, N. B., (1993). Allele frequencies at microsatellite loci: The stepwise mutation model revisited. Genetics 133, 737749.CrossRefGoogle ScholarPubMed
Weber, J. L., & May, P. E., (1989). Abundant class of human DNA polymorphisms which can be typed using the polymerase chain reaction. American Journal of Human Genetics 44, 388396.Google ScholarPubMed
Weber, J. L., & Wong, C., (1993). Mutation of human short tandem repeats. Human Molecular Genetics 2, 11231128.CrossRefGoogle ScholarPubMed
Willison, K. R., Dudley, K., & Potter, J., (1986). Molecular cloning and sequence analysis of a haploid expressed gene encoding t complex polypeptide-1. Cell 44, 727738.CrossRefGoogle ScholarPubMed