Skip to main content
×
×
Home

Genic differentiation and origin of Robertsonian populations of the house mouse (Mus musculus domesticus Rutty)

  • Janice Britton-Davidian (a1), Joseph H. Nadeau (a2), Henri Croset (a1) and Louis Thaler (a1)
Summary

This paper examines the relation between chromosomal and nuclear-gene divergence in 28 wild populations of the house mouse semi-species, Mus musculus domesticus, in Western Europe and North Africa. Besides describing the karyotypes of 15 of these populations and comparing them to those of 13 populations for which such information was already known, it reports the results of an electrophoretic survey of proteins encoded by 34 nuclear loci in all 28 populations. Karyotypic variation in this taxon involves only centric (or Robertsonian) fusions which often differ in arm combination and number between chromosomal races. The electrophoretic analysis showed that the amount of genic variation within Robertsonian (Rb) populations was similar to that for all-acrocentric populations, i.e. bearing the standard karyotype. Moreover, divergence between the two types of populations was extremely low. These results imply that centric fusions in mice have not modified either the level or the nature of genic variability. The genetic similarity between Rb and all-acrocentric populations is not attributed to the persistence of gene flow, since multiple fusions cause marked reproductive isolation. Rather, we attribute this extreme similarity to the very recent origin of chromosomal races in Europe. Furthermore, genic diversity measures suggest that geographically separated Rb populations have in situ and independent origins. Thus, Rb translocations are probably not unique events, but originated repeatedly. Two models are presented to explain how the rapid fixation of a series of chromosomal rearrangements can occur in a population without lowering variability in the nuclear genes. The first model assumes that chromosomal mutation rates are between 10−3 and 10−4 and that populations underwent a series of transient bottlenecks in which the effective population size did not fall below 35. In the second model, genic variability is restored following severe bottlenecks, through gene flow and recombination.

Copyright
References
Hide All
Adolph, S. & Klein, J. (1981). Robertsonian variation in Mus musculus from Central Europe, Spain and Scotland. Journal of Heredity 72, 219221.
Adolph, S. & Klein, J. (1983). Genetic variation of wild mouse populations in Southern Germany. I. Cytogenetic study. Genetical Research 41, 117134.
Baker, R. J. & Bickham, J. W. (1986). Speciation by monobrachial centric fusions. Proceedings of the National Academy of Sciences, USA 83, 82458248.
Berry, R. J. & Peters, J. (1977). Heterogeneous heterozygosities in Mus musculus populations. Proceedings of the Royal Society of London B 197, 485503.
Berry, R. J. & Peters, J. (1981). Allozymic variation in house mouse populations. In Mammalian Population Genetics (ed. Smith, M. H. and Joule, J.), pp. 242253. University of Georgia Press.
Bonhomme, F., Britton-Davidian, J., Thaler, L. & Trianta-phyllidis, C. (1978). Sur l'existence en Europe de quatre groupes de souris (genre Mus L.) du rang espèce et semi-espèce démontrée par la génétique biochimique. Comptes Rendus de l'Académie des Sciences, Paris 287, 631633.
Britton-Davidian, J. (1985). Différentiation génique et chromosomique chez les souris Mus musculus domesticus et Mus spretus. Relations avec la distribution spatiale des populations. Doctoral Thesis. USTL. Montpellier.
Britton-Davidian, J., Bonhomme, F., Croset, H., Capanna, E. & Thaler, L. (1980). Variabilité génétique chez les populations de souris (genre Mus L.) à nombre chromosomique réduit. Comptes Rendus de l'Académie des Sciences, Paris 290, 195198.
Brooker, P. C. (1982). Robertsonian translocations in Mus musculus from N.E. Scotland and Orkney. Heredity 48, 305309.
Capanna, E. (1982). Robertsonian numerical variation in animal speciation: Mus musculus, an emblematic model. In Mechanisms of Speciation (ed. Barigozzi, C.), pp. 155177. New York: Alan R. Liss.
Capanna, E., Civitelli, M. V. & Cristaldi, M. (1977). Chromosomal rearrangement, reproductive isolation and speciation in mammals. The case of Mus musculus. Bolletino di Zoologia 44, 213246.
Capanna, E., Corti, M. & Nascetti, G. (1985 a). Role of contact areas on chromosomal speciation of the European long-tailed house mouse (Mus musculus domesticus). Bolletino di Zoologia 52, 97119.
Capanna, E., Corti, M., Nascetti, G. & Bullini, L. (1985 b). Pre- and post-mating isolating mechanisms in the speciation of the European long-tailed house mouse Mus musculus domesticus. Acta Zoologica Fennica 170, 115120.
Cattanach, B. M. (1978). Crossover suppression in mice heterozygous for tobacco mouse metacentrics. Cytogenetics and Cell Genetics 20, 264281.
Chesser, R. K. & Baker, R. J. (1986). On factors affecting the fixation of chromosomal rearrangements and neutral genes: computer simulations. Evolution 40, 625632.
Corti, M., Capanna, E. & Estabrook, G. F. (1986). Microevolutionary sequences in house mouse chromosomal speciation. Systematic Zoology 35, 163175.
Ferris, S. D., Sage, R. D., Prager, E. M., Ritte, U. & Wilson, A. C. (1983). Mitochondrial DNA evolution in mice. Genetics 105, 681721.
Figueroa, F., Zaleska-Rutczynska, Z., Adolph, S., Nadeau, J. H. & Klein, J. (1982). Genetic variation of wild house mouse populations in Southern Germany. II. Serological study. Genetical Research 41, 135144.
Frykman, L., Simonsen, V. & Bengtsson, B. O. (1983). Genetic differentiation in Sorex. I. Electrophoretic analysis of the karyotypic races of Sorex araneus in Sweden. Hereditas 99, 279292.
Futuyma, D. J. & Mayer, G. C. (1980). Non-allopatric speciation in animals. Systematic Zoology 29, 254271.
Gropp, A. (1974). Animal model of human disease. American Journal of Pathology 77, 539542.
Gropp, A. & Kolbus, U. (1974). Exencephaly in the syndrome of trisomy n12 of the foetal mouse. Nature 249, 145147.
Gropp, A. & Winking, H. (1981). Robertsonian translocations: cytology, meiosis, segregation pattern and biological consequences of heterozygosity. Symposium of the Zoological Society of London 47, 141181.
Gropp, A., Winking, H., Redi, C., Capanna, E., Britton-Davidian, J. & Noack, G. (1982). Robertsonian karyotype variation in wild house mice from Rhaeto-Lombardia. Cytogenetics and Cell Genetics 34, 6777.
Harris, H. & Hopkinson, D. A. (1976). Handbook of Enzyme Electrophoresis. Amsterdam: North-Holland Press.
Harris, M. J., Wallace, M. E. & Evans, E. P. (1986). Aneuploidy in the embryonic progeny of females heterozygous for the Robertsonian chromosome (9.12) in genetically wild Peru-Coppock mice (Mus musculus). Journal of Reproduction and Fertility 76, 193203.
Hedrick, P. W. (1981). The establishment of chromosomal variants. Evolution 35, 322332.
Janossy, D. (1961). Die Entwicklung der Kleinsaugerfauna Europas im Pleistozan (Insectivora, Rodentia, Lagomorpha). Zeitschrift für Saugertierkunde 26, 164.
Lande, R. (1979). Effective deme sizes during long-term evolution estimated from rates of chromosomal rearrangement. Evolution 33, 234251.
Larson, A., Prager, E. M. & Wilson, A. C. (1984). Chromosomal evolution, speciation and morphological change in vertebrates: the role of social behaviour. Chromosomes Today 8, 215228.
Lee, M. R. & Elder, F. F. B. (1980). Yeast stimulation of bone marrow mitosis for cytogenetic investigation. Cytogenetics and Cell Genetics 26, 3640.
Lewontin, R. C. (1972). The apportionment of human diversity. Evolutionary Biology 6, 381398.
Moriwaki, K., Yonekawa, H., Gotch, O., Minezawa, M., Winking, H. & Gropp, A. (1984). Implications of the genetic divergence between European wild mice with Robertsonian translocations from the viewpoint of mitochondrial DNA. Genetical Research 43, 277287.
Mouse Newsletter. (1985). Mouse gene list. Volume 72: 2983.
Nadeau, J. H., Britton-Davidian, J., Bonhomme, B. & Thaler, L. (1988). H-2 polymorphisms are more uniformly distributed than allozyme polymorphisms in natural populations of the house mice. Genetics 118, 131140.
Nadeau, J. H., Wakeland, E. K., Gotze, D. & Klein, K. (1981). The population genetics of the H-2 polymorphism in European and North African populations of the house mouse (Mus musculus L.). Genetical Research 37, 1731.
Nash, H. R., Brooker, P. C. & Davis, S. J. M. (1983). The Robertsonian translocation house mouse populations of North East Scotland: a study of their origin and evolution. Journal of Heredity 50, 303310.
Nei, M. (1971). Interspecific gene differences and evolutionary time estimated from electrophoretic data on protein identity. American Naturalist 105, 385398.
Nei, M. (1978). Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89, 583590.
Nei, M., Maruyama, T. & Chakraborty, R. (1975). The bottleneck effect and genetic variability in populations. Evolution 29, 110.
Nesbitt, M. N. & Francke, U. (1973). A system of nomenclature for band patterns of mouse chromosomes. Chromosoma 41, 145158.
Pasteur, N., Pasteur, G., Bonhomme, F., Catalan, J. & Britton-Davidian, J. (1987). Manuel d'électrophorèse appliquée à la génétique des populations. Paris: Editions Techniques et Documentation.
Patton, J. L. & Sherwood, S. W. (1983). Chromosome evolution and speciation in rodents. Annual Review of Ecology and Systematics 14, 139158.
Qumsiyeh, M. B., Hamilton, M. J. & Schlitter, D. A. (1988). Problems in using Robertsonian rearrangements in determining monophyly: examples from the genera Tatera and Gerbillurus. Cytogenetics and Cell Genetics (In the Press).
Rogers, D. S., Greenbaum, I. F., Gunn, S. J. & Engstrom, M. D. (1984). Cytosystematic value of chromosomal inversion data in the genus Peromyscus (Rodentia: Cricetidae). Journal of Mammalogy 65, 457465.
Sage, R. D. (1981). Wild mice. In The Mouse in Biomedical Research vol. 1 (ed. Foster, H. L., Small, J. D. and Fox, J. G.), pp. 3990. New York: Academic Press.
Said, K., Jacquart, T., Montgelard, C., Sonjaya, H., Helal, A. N. & Britton-Davidian, J. (1986). Robertsonian house mouse populations in Tunisia: a karyotypical and biochemical study. Genetica 68, 151156.
Seabright, M. (1971). A rapid banding technique for human chromosomes. The Lancet ii, 971972.
Selander, R. K., Smith, M. H., Yang, S. Y., Johnson, W. E. & Gentry, J. B. (1971). IV. Biochemical polymorphism and systematics in the genus Peromyscus. I. Variation in the old-field mouse (Peromyscus polionotus). Studies in Genetics, University of Texas Publication 7103, 4990.
Shaw, D. D., Wilkinson, P. & Coates, D. J. (1983). Increased chromosomal mutation rate after hybridization between two subspecies of grasshoppers. Science 220, 11651167.
Sirkkomaa, S. (1983). Calculations on the decrease of genetic variation due to the founder effect. Hereditas 99, 1120.
Sites, J. W. & Moritz, C. (1987). Chromosomal evolution and speciation revisited. Systematic Zoology 36, 153174.
Spirito, F., Modesti, A., Perticone, P., Cristaldi, M., Federici, R. & Rizzoni, M. (1980). Mechanisms of fixation and accumulation of centric fusions in natural populations of Mus musculus L. I. Karyological analysis of a hybrid zone between two populations in the Central Apennines. Evolution 34, 453466.
Spirito, F., Rossi, C. & Rizzoni, M. (1983). Reduction of gene flow due to the partial sterility of heterozygotes for a chromosome mutation. I. Studies of a ‘neutral’ gene not linked to the chromosome mutation in a two population model. Evolution 37, 785797.
Tichy, H. & Vucak, I. (1987). Chromosomal polymorphism in the house mouse (Mus domesticus) of Greece and Yugoslavia. Chromosoma 95, 3136.
Walsh, J. B. (1982). Rate of accumulation of reproductive isolation by chromosome rearrangements. American Naturalist 120, 510532.
White, M. J. D. (1968). Models of speciation. Science 159, 10651070.
White, M. J. D. (1978). Chain processes in chromosomal speciation. Systematic Zoology 27, 285298.
Wilson, A. C., Cann, R. L., Carr, S. M., George, M., Gyllensten, U. B., Helm-Bychowski, K. M., Higuchi, R. G., Palumbi, S. R., Prager, E. M., Sage, R. D. & Stoneking, M. (1985). Mitochondrial DNA and two perspectives on evolutionary genetics. Biological Journal of the Linnean Society 26, 375400.
Winking, H. (1986). Some aspects of Robertsonian karyo-type variation in European wild mice. In Current Topics in Microbiology and Immunology 127, 6874.
Winking, H. & Gropp, A. (1976). Meiotic non-disjunction of metacentric heterozygotes in oocytes versus spermatocytes. In Ovulation in the Human, Proceedings of the Serono Symposium vol. 8 (ed. Crosignani, P. G. and Mishell, D. R.), pp. 4756. Academic Press.
Wright, S. (1965). The interpretation of population structure by F-statistics with special regard to systems of mating. Evolution 9, 395420.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Genetics Research
  • ISSN: 0016-6723
  • EISSN: 1469-5073
  • URL: /core/journals/genetics-research
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed