Skip to main content
Genetics logoLink to Genetics
. 1989 Jan;121(1):139–151. doi: 10.1093/genetics/121.1.139

Coevolution of the Major Histocompatibility Complex and the T-Complex in the Mouse. I. Generation and Maintenance of High Complementarity Associations

M K Uyenoyama 1
PMCID: PMC1203597  PMID: 2917711

Abstract

A quantitative model is developed to explore the effects of prezygotic and postzygotic incompatibility on the origin and maintenance of associations between the major histocompatibility complex (MHC) and the t-complex in the mouse. Incompatibility is represented by a reduction in the rate of conception or gestation of offspring derived from sperm bearing MHC antigens in common with the mother. Incompatibility encourages the evolution of associations from a state of complete independence between the two complexes by promoting the invasion of all novel antigens, including those that exhibit associations with the t-complex. Incompatibility can modify the relative numbers of antigens associated with each haplotype by actively promoting the exclusion or invasion of recombinants that bear formerly +-specific or t-specific antigens on the alternative haplotype. The results of the analysis indicate that the state of complete independence between the MHC and the t-complex is not preserved over evolutionary time in the presence of incompatibility. Further, the expression of incompatibility maintains fully associated states that include a single antigen associated with the t-haplotype and up to three to five antigens associated with the +-haplotype within a single population.

Full Text

The Full Text of this article is available as a PDF (1.1 MB).

Selected References

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

  1. Artzt K., Bennett D. Analogies between embryonic (T/t) antigens and adult major histocompatibility (H-2) antigens. Nature. 1975 Aug 14;256(5518):545–547. doi: 10.1038/256545a0. [DOI] [PubMed] [Google Scholar]
  2. 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]
  3. Chaouat G., Kolb J. P., Kiger N., Stanislawski M., Wegmann T. G. Immunologic consequences of vaccination against abortion in mice. J Immunol. 1985 Mar;134(3):1594–1598. [PubMed] [Google Scholar]
  4. Clarke A. G. The effects of maternal pre-immunization on pregnancy in the mouse. J Reprod Fertil. 1971 Mar;24(3):369–375. doi: 10.1530/jrf.0.0240369. [DOI] [PubMed] [Google Scholar]
  5. Clarke B., Kirby D. R. Maintenance of histocompatibility polymorphisms. Nature. 1966 Aug 27;211(5052):999–1000. doi: 10.1038/211999a0. [DOI] [PubMed] [Google Scholar]
  6. Cockerham C. C., Weir B. S. Sib mating with two linked loci. Genetics. 1968 Nov;60(3):629–640. doi: 10.1093/genetics/60.3.629. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. 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]
  8. Dunn L. C. EVIDENCE OF EVOLUTIONARY FORCES LEADING TO THE SPREAD OF LETHAL GENES IN WILD POPULATIONS OF HOUSE MICE. Proc Natl Acad Sci U S A. 1957 Jan 15;43(1):158–163. doi: 10.1073/pnas.43.1.158. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Franklin I., Lewontin R. C. Is the gene the unit of selection? Genetics. 1970 Aug;65(4):707–734. doi: 10.1093/genetics/65.4.707. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. 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]
  11. HULL P. EQUILIBRIUM OF GENE FREQUENCY PRODUCED BY PARTIAL INCOMPATIBILITY OF OFFSPRING WITH DAM. Proc Natl Acad Sci U S A. 1964 Mar;51:461–464. doi: 10.1073/pnas.51.3.461. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hammerberg C., Klein J. Linkage disequilibrium between H-2 and t complexes in chromosome 17 of the mouse. Nature. 1975 Nov 27;258(5533):296–299. doi: 10.1038/258296a0. [DOI] [PubMed] [Google Scholar]
  13. Hedrick P. W., Thomson G. Maternal-fetal interactions and the maintenance of HLA polymorphism. Genetics. 1988 May;119(1):205–212. doi: 10.1093/genetics/119.1.205. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. James D. A. Some effects of immunological factors on gestation in mice. J Reprod Fertil. 1967 Oct;14(2):265–275. doi: 10.1530/jrf.0.0140265. [DOI] [PubMed] [Google Scholar]
  15. Klein J., Figueroa F. Polymorphism of the mouse H-2 loci. Immunol Rev. 1981;60:23–57. doi: 10.1111/j.1600-065x.1981.tb00361.x. [DOI] [PubMed] [Google Scholar]
  16. Levinson J. R., McDevitt H. O. Murine t factors: an association between alleles at t and at H-2. J Exp Med. 1976 Sep 1;144(3):834–839. doi: 10.1084/jem.144.3.834. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. Nadeau J. H., Wakeland E. K., Götze D., Klein J. The population genetics of the H-2 polymorphism in European and North African populations of the house mouse (Mus musculus L.). Genet Res. 1981 Feb;37(1):17–31. doi: 10.1017/s0016672300019984. [DOI] [PubMed] [Google Scholar]
  19. 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]
  20. Shin H. S., Stavnezer J., Artzt K., Bennett D. Genetic structure and origin of t haplotypes of mice, analyzed with H-2 cDNA probes. Cell. 1982 Jul;29(3):969–976. doi: 10.1016/0092-8674(82)90460-3. [DOI] [PubMed] [Google Scholar]
  21. Silver L. M. Genomic analysis of the H-2 complex region associated with mouse t haplotypes. Cell. 1982 Jul;29(3):961–968. doi: 10.1016/0092-8674(82)90459-7. [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. Smith J. M., Haigh J. The hitch-hiking effect of a favourable gene. Genet Res. 1974 Feb;23(1):23–35. [PubMed] [Google Scholar]
  24. Snell G. D. The H-2 locus of the mouse: observations and speculations concerning its comparative genetics and its polymorphism. Folia Biol (Praha) 1968;14(5):335–358. [PubMed] [Google Scholar]
  25. Sturm S., Figueroa F., Klein J. The relationship between t and H-2 complexes in wild mice. I. The H-2 haplotypes of 20 t-bearing strains. Genet Res. 1982 Aug;40(1):73–88. doi: 10.1017/s0016672300018929. [DOI] [PubMed] [Google Scholar]
  26. Thomson G., Klitz W. Disequilibrium pattern analysis. I. Theory. Genetics. 1987 Aug;116(4):623–632. doi: 10.1093/genetics/116.4.623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Uyenoyama M. K. Coevolution of the major histocompatibility complex and the t-complex in the mouse. II. Modification of response to sharing of histocompatibility antigens. Genetics. 1989 Jan;121(1):153–161. doi: 10.1093/genetics/121.1.153. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Warburton F. E. Maintenance of histocompatibility polymorphisms. Heredity (Edinb) 1968 Feb;23(1):151–152. doi: 10.1038/hdy.1968.17. [DOI] [PubMed] [Google Scholar]
  29. 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]
  30. Wright S. The Distribution of Self-Sterility Alleles in Populations. Genetics. 1939 Jun;24(4):538–552. doi: 10.1093/genetics/24.4.538. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES