Reproductive isolation between chromosomal races of the house mouse Mus musculus domesticus in a parapatric contact area revealed by an analysis of multiple unlinked loci

Journal of Evolutionary Biology

Volumn 21, Issue 2, 2008, Pages 502-513

  Franchini, P ^a   Castiglia, R ^a   Capanna, E ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

Chromosomal races; Gene flow; House mouse; Hybrid zone; Microsatellite; Reproductive isolation

Indexed keywords

MICROSATELLITE DNA;

CHROMOSOME; GENE FLOW; GENETIC DIFFERENTIATION; GENOTYPE; HYBRID; PARAPATRY; POPULATION GENETICS; REPRODUCTIVE ISOLATION; RODENT; SPECIATION (BIOLOGY);

ANIMAL; ARTICLE; CHROMOSOME; CHROMOSOME ABERRATION; GENE FLOW; GENETICS; MOUSE; SPECIES DIFFERENTIATION;

ANIMALS; CHROMOSOME ABERRATIONS; CHROMOSOMES, MAMMALIAN; GENE FLOW; GENETIC SPECIATION; MICE; MICROSATELLITE REPEATS;

MUS; MUS MUSCULUS; MUS MUSCULUS DOMESTICUS; ROBERTSONIA; RODENTIA;

EID: 38849103145     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/j.1420-9101.2007.01492.x     Document Type: Article

References (54)

1. Anderson, E.C. Thompson, E.A. 2002. A model-based method for identifying species hybrids using multilocus genetic data. Genetics 160 : 1217 1229.
2. Andersson, A.C., Narain, Y., Tegelström, H. Fredga, K. 2004. No apparent reduction of gene flow in a hybrid zone between the West and North European karyotypic groups of the common shrew, Sorex araneus. Mol. Ecol. 13 : 1205 1215.
3. Auffray, J.-C., Vanlerberghe, F. Britton-Davidian, J. 1990. The house mouse progression in Eurasia: a palaeontological and archaeozoological approach. Biol. J. Linn. Soc. 41 : 13 25.
4. Basset, P., Yannic, G., Brünner, H. Hausser, J. 2006. Restricted gene flow at specific parts of the shrew genome in chromosomal hybrid zones. Evolution 60 : 1718 1730.
5. Belkhir, K., Borsa, P., Chikhi, L., Raufaste, N. Bonhomme, F. 2004. genetix 4.05, Logiciel Sous WindowsTM Pour la Gènètique Des Populations. Laboratoire Gènome, Populations, Interactions, CNRS UMR 5000, Universitè de Montpellier II, France.
6. Benzécri, J.P. 1973. L'analyse des Données. Tome 1: La Taxinomie; Tome II: L'analyse des Correspondences. Dunod, Paris.
7. Bidau, C.J., Giménez, M.D., Palmer, C.L. Searle, J.B. 2001. The effects of Robertsonian fusions on chiasma frequency and distribution in the house mouse (Mus musculus domesticus) from a hybrid zone in northern Scotland. Heredity 87 : 305 313.
8. Britton-Davidian, J., Catalan, J., Ramalhinho, M.G., Ganem, G., Auffray, J.-C., Capela, R., Biscoito, M., Searle, J.B. Mathias, M.L. 2000. Rapid chromosomal evolution in island mice. Nature 403 : 158.
9. Capanna, E. 1982. Robertsonian numerical variation in animal speciation: Mus musculus, an emblematic model. In : Mechanism of Speciation (C. Barigozzi, ed pp. 155 177. Alan Liss, New York.
10. Capanna, E., Corti, M., Mainardi, D., Parmigiani, S. Brain, P.F. 1984. Karyotype and intermale aggression in wild house mice: ecology and speciation. Behav. Genet. 14 : 195 208.
11. Carpineti, M. Castiglia, R. 2004. Analysis of behavioural discrimination mechanisms in a contact zone between two metacentric races of the house mouse, Mus musculus domesticus, in central Italy. Rend. Fis. Acc. Lincei 15 : 31 41.
12. Castiglia, R. Capanna, E. 1999a. Contact zones between chromosomal races of Mus musculus domesticus. 1. Temporal analysis of hybrid zone between the CD chromosomal race (2n = 22) and populations with the standard karyotype. Heredity 83 : 319 326.
13. Castiglia, R. Capanna, E. 1999b. Whole-arm reciprocal translocation (WART) in a feral population of mice. Chromosome Res. 7 : 493 495.
14. Castiglia, R. Capanna, E. 2000. Contact zone between chromosomal races of Mus musculus domesticus. 2. Fertility and segregation in laboratory-reared and wild mice heterozygous for multiple Robertsonian rearrangements. Heredity 85 : 147 156.
15. Castiglia, R. Capanna, E. 2002. Chiasma repatterning across a chromosomal hybrid zone between chromosomal races of Mus musculus domesticus. Genetica 114 : 35 40.
16. Castiglia, R., Annesi, F. Capanna, E. 2002. Contact zones between chromosomal races of Mus musculus domesticus. 3. Molecular and chromosomal evidence of restricted gene flow between the CD race (2n = 22) and the ACR race (2n = 24). Heredity 89 : 219 224.
17. Chatti, N., Britton-Davidian, J., Catalan, J., Auffray, J. Said, K. 2005. Reproductive trait divergence and hybrid fertility patterns between chromosomal races of the house mouse in Tunisia: analysis of wild and laboratory-bred males and females. Biol. J. Linn. Soc. 84 : 407 416.
18. Cucchi, T., Vigne, J.D. Auffray, J.-C. 2005. First occurrence of the house mouse (Mus musculus domesticus Schwarz & Schwarz, 1943) in the Western Mediterranean: a zooarchaeological revision of sub-fossil house mouse occurrences. Biol. J. Linn. Soc. 84 : 429 445.
19. Dallas, J.F., Bonhomme, F., Boursot, P., Britton-Davidian, J. Bauchau, V. 1998. Population genetic structure in a Robertsonian race of house mice: evidence from microsatellite polymorphism. Heredity 80 : 70 77.
20. Davisson, M.T. 1996. Rules and guidelines for gene nomenclature. In : Genetic Variants and Strains of the Laboratory Mouse (M. F. Lyon, S. Rastan S. D. M. Brown, eds pp. 1 16. Oxford University Press, Oxford, UK.
21. Evanno, G., Regnaut, S. Goudet, J. 2005. Detecting the number of clusters of individuals using the software Structure: a simulation study. Mol. Ecol. 14 : 2611 2620.
22. Excoffier, L., Laval, G. Schneider, S. 2005. Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol. Bioinform. Online 1 : 47 50.
23. Falush, D., Stephens, M. Pritchard, J.K. 2003. Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164 : 1567 1587.
24. Gaggiotti, O.E., Lange, O., Rassmann, K. Gliddon, C. 1999. A comparison of two indirect methods for estimating average levels of gene flow using microsatellite data. Mol. Ecol. 8 : 1513 1520.
25. Goodman, S.J. 1997. rst calc: a collection of computer programs for calculating unbiased estimates of genetic differentiation and determining their significance for microsatellite data. Mol. Ecol. 6 : 881 885.
26. Goudet, J. 2001. fstat, a Program to Estimate and Test Gene Diversities and Fixation Indices (Version 2.9.3). Institut d'Ecologie, Bâtiment de Biologie, Université de Lausanne, Switzerland.
27. Goudet, J., Raymond, M., De Meeüs, T. Rousset, F. 1996. Testing differentiation in diploid populations. Genetics 144 : 1933 1940.
28. Gropp, A., Tettenborn, U. Von Lehmann, E. 1969. Chromosomenvariation von Robertson'schen typus bei der tabakmaus, Mus poschiavinus, und ihren hybriden mit der laboratoriusmaus. Cytogenetics 9 : 9 23.
29. Guo, S.W. Thompson, E.A. 1992. Performing the exact test of Hardy-Weinberg proportions for multiple alleles. Biometrics 48 : 361 372.
30. Hartl, D.L. Clark, A.G. 1997. Principles of Population Genetics. Sinauer, Sunderland, MA.
31. Hauffe, H.C. Searle, J.B. 1992. A disappearing speciation event? Nature 357 : 26.
32. Hauffe, H.C. Searle, J.B. 1998. Chromosomal heterozygosity and fertility in house mice (Mus musculus domesticus) from Northern Italy. Genetics 150 : 1143 1154.
33. King, M. 1993. Species Evolution, the Role of Chromosome Change. Cambridge University Press, Cambridge.
34. Louis, E.J. Dempster, E.R. 1987. An exact test for Hardy-Weinberg and multiple alleles. Biometrics 43 : 805 811.
35. Lugon-Moulin, N., Balloux, F. Hausser, J. 2000. Genetic differentiation of common shrew Sorex araneus populations among different alpine valleys revealed by microsatellites. Acta Theriol. 45 : 103 117.
36. Malorni, W., Capanna, E., Cristaldi, M. De Martino, E. 1982. Changes of seminiferous epithelium in hybrids of mice carrying Robertsonian karyotype. Arch. Androl. 9 : 333 341.
37. Moritz, C. 1994. Defining 'Evolutionarily Significant Units' for conservation. Trends Ecol. Evol. 9 : 373 375.
38. Panithanarak, T., Hauffe, H.C., Dallas, J.F., Glover, A., Ward, R.G. Searle, J.B. 2004. Linkage-dependent gene flow in a house mouse chromosomal hybrid zone. Evolution 58 : 184 192.
39. Piálek, J., Hauffe, H.C. Searle, J.B. 2005. Chromosomal variation in the house mouse. Biol. J. Linn. Soc. 84 : 535 563.
40. Piry, S., Alapetite, A., Cornuet, J.M., Paetkau, D., Baudouin, L. Estoup, A. 2004. Geneclass 2: a software for genetic assignment and first-generation migrant detection. J. Hered. 95 : 536 539.
41. Pritchard, J.K., Stephens, M. Donnelly, P.J. 2000. Inference of population structure using multilocus genotype data. Genetics 155 : 945 959.
42. Raymond, M. Rousset, F. 1995. genepop (version 1.2): population genetics software for exact tests and ecumenicism. J. Hered. 86 : 248 249.
43. Redi, C.A. Capanna, E. 1988. Robertsonian heterozygotes in the house mouse and the fate of their germ cells. In : The Cytogenetics of Mammalian Autosomal Rearrangements (A. Daniel, ed pp. 315 359. Alan Liss, New York.
44. Reich, D.E., Feldman, M.W. Goldstein, D.B. 1999. Statistical properties of two tests that use multilocus data sets to detect population expansions. Mol. Biol. Evol. 16 : 453 466.
45. Rieseberg, L.H. 2001. Chromosomal rearrangements and speciation. Trends Ecol. Evol. 16 : 351 358.
46. Rousset, F. 1997. Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145 : 1219 1228.
47. Sage, R.D., Atchley, W.R. Capanna, E. 1993. House mice as models in systematic biology. Syst. Biol. 42 : 523 561.
48. Searle, J.B. 1993. Chromosomal hybrid zones in eutherian mammals. In : Hybrid Zones and the Evolutionary Process (R. G. Harrison, ed pp. 309 353. Oxford University Press, New York.
49. Slatkin, M. 1995. A measure of population subdivision based on microsatellite allele frequencies. Genetics 139 : 457 462.
50. Vaha, J.P. Primmer, C.R. 2006. Efficiency of model-based Bayesian methods for detecting hybrid individuals under different hybridization scenarios and with different numbers of loci. Mol. Ecol. 15 : 63 72.
51. Weir, B.S. Cockerham, C.C. 1984. Estimating F-statistics for the analysis of population structure. Evolution 38 : 1358 1370.
52. White, M.J.D. 1978. Modes of Speciation. W.H. Freeman & Co., San Francisco.
53. Wilson, G.A. Rannala, B. 2003. Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163 : 1177 1191.
54. Wright, S. 1951. The genetical structure of populations. Ann. Eugen. 15 : 313 354.