Abstract
Comparison of the rate of synonymous and nonsynonymous nucleotide substitutions suggests that certain regions of the functional H-2 genes, which are part of the mouse major histocompatibility complex (Mhc), are under strong positive selection pressure. Thus far, however, little evidence has been provided for the existence of such pressure in natural mouse populations. We have, therefore, initiated experiments designed to test the hypothesis of positive selection acting on H-2 loci. The experiments are being carried out on two natural mouse populations in Jerusalem, Israel. One population occupies a space of about 100 m2 in a chicken coop, the other lives in a nearby field in which “mouse stations” providing food and shelter have been set up. Extensive typing of these two populations revealed the presence of only four H-2 haplotypes. Mice in the two populations breed continually all year around, yet population size varies seasonally, with population maxima in winter and minima in summer. The population in the chicken coop contains a relatively stable nucleus which may be organized in demes with an excess of females over males and limited territorial mobility. The rest of the mice stay in the population for a short time only and then either die or emigrate. The field population is smaller and more loosely organized than the chicken-coop population, with demes probably forming only during population maxima. For the rest of the time breeding in this population is probably panmictic. At a population minimum in the summer of 1984, H-2 homozygotes happened to predominate over heterozygotes. This situation, however, lasted for a short time only and thereafter there was a continuous, statistically highly significant increase in the proportion of H-2 heterozygotes of one or two types. The increase occurred in both populations but was more apparent in the chicken-coop population. This observation provides the first experimental evidence that heterozygous advantage might be one of the mechanisms maintaining high H-2 polymorphism in natural populations of the house mouse.
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References
Andrzejewski, R., Petrusewicz, K., and Walkowa, W.: Preliminary report on results obtained with a living trap in a confined population of mice. Bull Acad Pol Sci 7: 367–370, 1959
Berry, R. J.: The ecology of an island population of the house mouse. J Anim Ecol 37: 445–470, 1968
Berry, R. J.: Genetic processes in wild mouse populations. Past myth and present knowledge. In M. Potter, J. H. Nadeau, and M. P. Cancro (eds.): The Wild Mouse in Immunology. Current Topics in Microbiology and Immunology, vol. 127, pp. 86–94, Springer Verlag, New York, 1986
Berry, R. J. and Jakobson, M.: Life and death in an island population of the house mouse. Exp Gerontol 6: 187–197, 1971
Bjorkman, P. J., Saper, M. A., Samraoui, B., Bennett, W. S., Strominger, J. L., and Wiley, D. C.: The foreign antigen binding site and T cell recognition regions of class I histocompatibility antigens. Nature 329: 512–518, 1987
Black, F. L. and Salzano, F. M.: Evidence for heterosis in the HLA system. Am J Hum Genet 33: 894–899, 1981
Bronson, F. H.: The reproductive biology of the house mouse. Q Rev Biol 54: 265–299, 1979
Brown, R. Z.: Social behaviour, reproduction and population changes in the house mouse (Mus musculus L.). Ecol Monogr 36: 627–634, 1953
Brown, J. H., Jerdetzky, T., Saper, M. A., Samraoui, B., Bjorkman, P. J., and Wiley, D. C.: A hypothetical model of the foreign antigen binding site of class II histocompatibility molecules. Nature 332: 845–850, 1988
Crowcroft, P. and Rowe, F. P.: Social organization and territorial behaviour in the wild house mouse (Mus musculus L.). Proc Zool Soc London 140: 517–531, 1963
Degos, L., Colombani, J., Chaventre, A., Bengston, B., and Jacquard, A.: Selective pressure on HLA polymorphism. Nature 249: 62–63, 1974
DeLong, K. T.: Population ecology of feral house mice. Ecology 48: 611–634, 1967
Hedrick, P. W. and Thomson, G.: Evidence for balancing selection at HLA. Genetics 104: 449–456, 1983
Hughes, A. L. and Nei, M.: Pattern of nucleotide substitutions at major histocompatibility complex class I loci reveals overdominant selection. Nature 335: 167–170, 1988
Hughes, A. L. and Nei, M.: Nucleotide substitution at major histocompatibility complex class II loci: Evidence for overdominant selection. Proc Natl Acad Sci USA 86: 958–962, 1989
Jonsson, A.-K., Andersson, L., and Rask, L.: Selection for polymorphism in the antigen recognition site of major histocompatibility complex class II molecules. Scand J Immunol 30: 409–417, 1989
Justice, K. E.: Ecological and genetical studies of evolutionary forces acting on desert populations of Mus musculus. Arizona-Sonora Desert Museum Inc., Tucson, 1962
Klein, J.: Natural History of the Major Histocompatibility Complex. John Wiley, New York, 1986
Klein, J. and Figueroa, F.: Evolution of the major histocompatibility complex. CRC Crit Rev Immunol 6: 295–386, 1986
Lewontin, R. C. and Dunn, L. C.: The evolutionary dynamics of a polymorphism in the house mouse. Genetics 45: 705–722, 1960
Lidicker, W. Z.: Comparative study of density regulation in confined populations of four species of rodents. Res Popul Ecol 7: 57–72, 1965
Lidicker, W. Z.: Ecological observations on a feral house mouse population declining to extinction. Ecol Monogr 36: 27–50, 1966
Myers, J. H.: Genetic and social structure of feral house populations on Grizzly Island, California. Ecology 55: 747–759, 1974
Neufeld, E., Ritte, U., Figueroa, F., and Klein, J.: Low H-2 polymorphism in some Israeli wild mouse populations. Immunogenetics 24: 374–380, 1986
Osborne, W. A.: Mice plagues in Australia. Nature 129: 755, 1932
Petras, M. L.: Studies on natural populations of Mus. I. Biochemical polymorphisms and their bearing on population structure. Evolution 21: 259–274, 1967
Petrusewicz, K.: Further investigation of the influence exerted by the presence of their home cages and own populations on the results of fights between male mice. Bull Acad Pol Sci 7: 319–326, 1959
Reimer, J. D. and Petras, M. L.: Breeding structure of the house mouse, Mus musculus, in a population cage. J Mammal 48: 88–99, 1967
Selander, R. K.: Behavior and genetic variation in natural populations. Am Zool 10: 43–52, 1979
Singleton, G. R.: The social and genetic structure of a natural colony of house mice, Mus musculus, at Healesville wildlife sanctuary. Aust J Zool 31: 155–166, 1983
Southwick, C. H.: The population dynamics of confined house mice supplied with unlimited food. Ecology 36: 212–225, 1955
Stueck, K. L. and Barrett, G. W.: Effects of resource partitioning on the population dynamics and energy utilization strategies of feral house mouse (Mus musculus) populations under experimental field conditions. Ecology 59: 539–551, 1978
Takahata, N. and Nei, M.: Allelic genealogy under overdominant and frequency-dependent selection and polymorphism of major of major histocompatibility complex loci. Genetics 124: 967–978, 1990
Young, H., Strecker, R. L., and Eulen, J. T. Jr.: Localization of activity in two indoor populations of house mice Mus musculus. J Mammal 31: 403–410, 1950
Zalenska-Rutczynska, Z., Figueroa, F., and Klein, J.: Sixteen new H-2 haplotypes derived from wild mice. Immunogenetics 18: 189–206, 1983
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Ritte, U., Neufeld, E., O'hUigin, C. et al. Origins of H-2 polymorphism in the house mouse. II. characterization of a model population and evidence for heterozygous advantage. Immunogenetics 34, 164–173 (1991). https://doi.org/10.1007/BF00205819
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DOI: https://doi.org/10.1007/BF00205819