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

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.

[1]  S. Sirkkomaa.  Calculations on the decrease of genetic variation due to the founder effect. , 2008, Hereditas.

[2]  B. Bengtsson,et al.  Genetic differentiation in Sorex. I. Electrophoretic analysis of the karyotypic races of Sorex araneus in Sweden. , 2008, Hereditas.

[3]  Craig Moritz,et al.  Chromosomal Evolution and Speciation Revisited , 1987 .

[4]  R. Baker,et al.  Speciation by monobrachial centric fusions. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[5]  G. Estabrook,et al.  MICROEVOLUTIONARY SEQUENCES IN HOUSE MOUSE CHROMOSOMAL SPECIATION , 1986 .

[6]  R. Baker,et al.  ON FACTORS AFFECTING THE FIXATION OF CHROMOSOMAL REARRANGEMENTS AND NEUTRAL GENES: COMPUTER SIMULATIONS , 1986, Evolution; international journal of organic evolution.

[7]  M. Stoneking,et al.  Mitochondrial DNA and two perspectives on evolutionary genetics , 1985 .

[8]  M. Engstrom,et al.  Cytosystematic Value of Chromosomal Inversion Data in the Genus Peromyscus (Rodentia: Cricetidae) , 1984 .

[9]  O. Gotoh,et al.  Implications of the genetic divergence between European wild mice with Robertsonian translocations from the viewpoint of mitochondrial DNA. , 1984, Genetical research.

[10]  A. Wilson,et al.  Mitochondrial DNA evolution in mice. , 1983, Genetics.

[11]  S. Sherwood,et al.  Chromosome evolution and speciation in rodents , 1983 .

[12]  M. Rizzoni,et al.  REDUCTION OF GENE FLOW DUE TO THE PARTIAL STERILITY OF HETEROZYGOTES FOR A CHROMOSOME MUTATION. I. STUDIES ON A “NEUTRAL” GENE NOT LINKED TO THE CHROMOSOME MUTATION IN A TWO POPULATION MODEL , 1983, Evolution; international journal of organic evolution.

[13]  D. Coates,et al.  Increased chromosomal mutation rate after hybridization between two subspecies of grasshoppers. , 1983, Science.

[14]  H. Nash,et al.  The Robertsonian translocation house-mouse populations of North East Scotland: a study of their origin and evolution , 1983, Heredity.

[15]  J. Klein,et al.  Genetic variation of wild mouse populations in southern Germany. II. Serological study. , 1983, Genetical research.

[16]  J. Klein,et al.  Genetic variation of wild mouse populations in southern Germany. I. Cytogenetic study. , 1983, Genetical research.

[17]  J. B. Walsh,et al.  Rate of Accumulation of Reproductive Isolation by Chromosome Rearrangements , 1982, The American Naturalist.

[18]  P. Brooker.  Robertsonian translocations in Mus musculus from N.E. Scotland and Orkney , 1982, Heredity.

[19]  J. Klein,et al.  Robertsonian variation in Mus musculus from Central Europe Spain, and Scotland. , 1981, The Journal of heredity.

[20]  P. Hedrick.  THE ESTABLISHMENT OF CHROMOSOMAL VARIANTS , 1981, Evolution; international journal of organic evolution.

[21]  J. Klein,et al.  The population genetics of the H-2 polymorphism in European and North African populations of the house mouse (Mus musculus L.). , 1981, Genetical research.

[22]  D. Futuyma,et al.  Non-Allopatric Speciation in Animals , 1980 .

[23]  M. Cristaldi,et al.  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 , 1980, Evolution; international journal of organic evolution.

[24]  R. Lande.  EFFECTIVE DEME SIZES DURING LONG‐TERM EVOLUTION ESTIMATED FROM RATES OF CHROMOSOMAL REARRANGEMENT , 1979, Evolution; international journal of organic evolution.

[25]  M. White.  Chain Processes in Chromosomal Speciation , 1978 .

[26]  M. Nei,et al.  Estimation of average heterozygosity and genetic distance from a small number of individuals. , 1978, Genetics.

[27]  R. Berry,et al.  Heterogeneous heterozygosities in Mus musculus populations , 1977, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[28]  Lofland Hb.  Animal model of human disease. , 1975, The American journal of pathology.

[29]  M. Nei,et al.  THE BOTTLENECK EFFECT AND GENETIC VARIABILITY IN POPULATIONS , 1975, Evolution; international journal of organic evolution.

[30]  A. Gropp.  Animal model of human disease. Autosomal trisomy, developmental impairment and fetal death. , 1974, The American journal of pathology.

[31]  A. Gropp,et al.  Exencephaly in the syndrome of trisomy No. 12 of the foetal mouse , 1974, Nature.

[32]  M. Seabright.  A rapid banding technique for human chromosomes. , 1971, Lancet.

[33]  M. Nei.  Interspecific Gene Differences and Evolutionary Time Estimated from Electrophoretic Data on Protein Identity , 1971, The American Naturalist.

[34]  M J White,et al.  Models of speciation. New concepts suggest that the classical sympatric and allopatric models are not the only alternatives. , 1968, Science.

[35]  S. Wright.  THE INTERPRETATION OF POPULATION STRUCTURE BY F‐STATISTICS WITH SPECIAL REGARD TO SYSTEMS OF MATING , 1965 .

[36]  Mouse Genome.  Mouse gene list. , 1990 .

[37]  F. Bonhomme,et al.  H-2 polymorphisms are more uniformly distributed than allozyme polymorphisms in natural populations of house mice. , 1988, Genetics.

[38]  M. Qumsiyeh,et al.  Problems in using Robertsonian rearrangements in determining monophyly: examples from the genera Tatera and Gerbillurus. , 1987, Cytogenetics and cell genetics.

[39]  M. J. Harris,et al.  Aneuploidy in the embryonic progeny of females heterozygous for the Robertsonian chromosome (9.12) in genetically wild Peru-Coppock mice (Mus musculus). , 1986, Journal of reproduction and fertility.

[40]  H. Winking.  Some aspects of Robertsonian karyotype variation in European wild mice. , 1986, Current topics in microbiology and immunology.

[41]  G. Nascetti,et al.  Role of contact areas in chromosomal speciation of the European long-tailed house mouse (Mus musculus domesticus) , 1985 .

[42]  A. Wilson,et al.  Chromosomal evolution, speciation and morphological change in vertebrates: the role of social behaviour , 1984 .

[43]  C. Redi,et al.  Robertsonian karyotype variation in wild house mice from Rhaeto-Lombardia. , 1982, Cytogenetics and cell genetics.

[44]  E. Capanna.  Robertsonian numerical variation in animal speciation: Mus musculus, an emblematic model. , 1982, Progress in clinical and biological research.

[45]  Michael H. Smith,et al.  Mammalian population genetics , 1981 .

[46]  F. Elder,et al.  Yeast stimulation of bone marrow mitosis for cytogenetic investigations. , 1980, Cytogenetics and cell genetics.

[47]  B. Cattanach.  Crossover suppression in mice heterozygous for tobacco mouse metacentrics. , 1978, Cytogenetics and cell genetics.

[48]  Cattanach Bm.  Crossover suppression in mice heterozygous for tobacco mouse metacentrics. , 1978 .

[49]  M. Cristaldi,et al.  Chromosomal Rearrangement, Reproductive Isolation and Speciation in Mammals. The Case of Mus Musculus , 1977 .

[50]  E. Giblett.  Handbook of enzyme electrophoresis in human genetics , 1977 .

[51]  R. Lewontin.  The Apportionment of Human Diversity , 1972 .

[52]  R. Selander.  Biochemical polymorphism and systemics in the genus Peromyscus. I. Variation in the old-field mouse (Peromyscus polionotus) , 1971 .

[53]  D. Jánossy.  Die Entwicklung der Kleinsäugerfauna Europas im Pleistozän (Insectivora, Rodentia, Lagomorpha) , 1961 .