Differential patterns of introgression across the X chromosome in a hybrid zone between two species of house mice

Evolution

Volumn 58, Issue 9, 2004, Pages 2064-2078

  Payseur, Bret A ^a,b   Krenz, James G ^a,c   Nachman, Michael W ^a  

^a University of Arizona   (United States)

^b Department of Obstetrics Gynecology   (United States)

^c AGRICULTURAL RESEARCH SERVICE   (United States)

Author keywords

Cline; Gene flow; Mammals; Reproductive isolation; Speciation

Indexed keywords

CLINE; GENE FLOW; HYBRID ZONE; HYBRIDIZATION; INTROGRESSION; RODENT; SPECIATION (BIOLOGY);

ANIMALIA; MAMMALIA; MUS; MUS DOMESTICUS; MUS MUSCULUS; MUS MUSCULUS DOMESTICUS; MUSCULUS; RODENTIA;

EID: 5344240384     PISSN: 00143820     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.0014-3820.2004.tb00490.x     Document Type: Article

References (84)

1. Ammerman, A. J., and L. L. Cavalli-Sforza. 1984. The Neolithic transition and the genetics of populations in Europe. Princeton Univ. Press, Princeton, NJ.
2. Arnold, M. L. 1997. Natural hybridization and evolution. Oxford Univ. Press, New York.
3. Barbash, D. A., D. F. Siino, A. M. Tarone, and J. Roote. 2003. A rapidly evolving MYB-related protein causes species isolation in Dmsophila. Proc. Natl. Acad. Sci. USA 100:5302-5307.
4. Barton, N. H. 1983. Multilocus clines. Evolution 37:454-471.
5. Barton, N. H., and K. S. Gale. 199.3. Genetic analysis of hybrid zones. Pp. 13-45 in R. G. Harrison, ed. Hybrid zones and the evolutionary process. Oxford Univ. Press, Oxford, U.K.
6. Barton, N. H., and G. M. Hewitt. 1985. Analysis of hybrid zones. Annu. Rev. Ecol. Syst. 16:113-148.
7. Bateson, W. 1909. Heredity and variation in modern lights. Pp. 85-101 in A. C. Seward, ed. Darwin and modern science. Cambridge Univ. Press, Cambridge, U.K.
8. Bazykin, A. D. 1969. Hypothetical mechanism of speciation. Evolution 23:685-687.
9. Bishop, C. E., P. Boursot, B. Baron, F. Bonhomme, and D. Hatat. 1985. Most classical Mus musculus domesticus laboratory mouse strains carry a Mus musculus musculus Y chromosome. Nature 325:70-72.
10. Boursot, P., J.-C. Auffray, J. Britton-Davidian, and F. Bonhomme. 1993. The evolution of house mice. Annu. Rev. Ecol. Syst. 24: 119-152.
11. Christie, P., and M. R. Macnair. 1984. Complementary lethal factors in two North American populations of the yellow monkeyflower. J. Hered. 75:510-511.
12. Coyne, J. A., and H. A. Orr. 1989. Two rules of speciation. Pp. 180-207 in D. Otte and J. Endler, eds. Speciation and its consequences. Sinauer Associates, Sunderland, MA.
13. Crow, J. F. 1942. Cross fertility and isolating mechanisms in the Drosophila mulleri group. Univ. Texas Pub. 4228:53-67.
14. Dietrich, W. F., J. Miller. R. Steen, M. A. Merchant, D. Damron-Boles, Z. Husain, R. Dredge, M. J. Daly, K. A. Ingalls, T. J. O'Connor, C. A. Evans, M. M. DeAngelis, D. M. Levinson, L. Kruglyak, N. Goodman, N. G. Copeland, N. A. Jenkins, T. L. Hawkins, L. Stein, D. C. Page, and E. S. Lander. 1996. A comprehensive genetic map of the mouse genome. Nature 380: 149-152.
15. Dobzhansky, T. 1936. Studies on hybrid sterility. II. Localization of sterility factors in Drosophila pseudoobscura hybrids. Genetics 21:113-135.
16. Dod, B., L. S. Jermiin, P. Boursot, V. H. Chapman, J. Tonnes-Nielsen, and F. Bonhomme. 1993. Counterselection on sex chromosomes in the Mus musculus European hybrid zone. J. Evol. Biol. 6:529-546.
17. Edwards, A. W. F. 1992. Likelihood. Johns Hopkins Univ. Press. Baltimore, MD.
18. Endler, J. A. 1977. Geographic variation, speciation, and clines. Princeton Univ. Press, Princeton, NJ.
19. Ferris, S. D., R. D. Sage, and A. C. Wilson. 1982. Evidence from mtDNA sequences that common laboratory strains of inbred mice are descended from a single female. Nature 295:163-165.
20. Forejt, J. 1996. Hybrid sterility in the mouse. Trends Genet. 12: 412-417.
21. Forejt, J., and P. Ivanyi. 1975. Genetic studies on male sterility of hybrids between laboratory and wild mice (Mus musculus L.). Genet. Res. 24:189-206.
22. Grula, J. W., and O. R. Taylor. 1982. Some characteristics of hybrids derived from the sulfur butterflies, Collas eurytheme and Colias philodice: phenotypic effects of the X chromosome. Evolution 34:673-687.
23. Hagen, R. H. 1990. Population structure and host use in hybridizing subspecies of Papilio glaucus (Lepidoptera: Papilionidae). Evolution 44:1914-1930.
24. Haldane, J. B. S. 1922. Sex-ratio and unisexual sterility in hybrid animals. J. Genet. 12:101-109.
25. Harrison, R. G. 1990. Hybrid zones: windows on evolutionary process. Oxf. Surv. Evol. Biol. 7:69-128.
26. Hill, W. G. 1974. Estimation of linkage disequilibrium in randomly mating populations. Heredity 33:229-239.
27. Hollingshead, L. 1930. A lethal factor in Crepis effective only in interspecific hybrids. Genetics 15:114-140.
28. Hunt, W. G., and R. K. Selander. 1973. Biochemical genetics of hybridisation in European house mice. Heredity 31:11-33.
29. Jiggins, C. D., M. Linares, R. E. Naisbit, C. Salazar, Z. H. Yang, and J. Mallet. 2001. Sex-linked hybrid sterility in a butterfly. Evolution 55:1631-1638.
30. Laurie, C. C. 1997. The weaker sex is heterogametic: 75 years of Haldane's rule. Genetics 147:937-951.
31. Lewontin, R. C. 1964. The interaction of selection and linkage. I. General considerations; heterotic models. Genetics 49:49-67.
32. Lindblad-Toh, K., E. Winchester, M. J. Daly, D. G. Wang, J. N. Hirschhorn, J. P. Laviolette, K. Ardlie, D. E. Reich, E. Robinson, P. Sklar, N. Shah, D. Thomas, J. B. Fan, T. Gingeras, J. Warrington, N. Patil, T. J. Hudson, and E. S. Lander. 2000. Large-scale discovery and genotyping of single-nucleotide polymorphisms in the mouse. Nat. Genet. 24:381-386.
33. Macholan, M. 1996. Morphometric analysis of European house mice. Acta Theriol. 41:255-275.
34. Malitschek, B., D. Fornzler, and M. Schartl. 1995. Melanoma formation in Xiphophorus: a model system for the role of receptor tyrosine kinases in tumorigenesis. Bioessays 17:1017-1023.
35. Martinsen, G. D., T. G. Whitham, R. J. Turek, and P. Keim. 2001. Hybrid populations selectively filter gene introgression between species. Evolution 55:1325-1335.
36. Moulia, C., N. LeBrun, J. Dallas, A. Orth, and F. Renaud. 1993. Experimental evidence of genetic determinism in high susceptibility to intestinal pinworm infection in mice: a hybrid zone model. Parasitology 106:387-393.
37. Moulia, C., N. LeBrun, C. Loubes, R. Marin, and F. Renaud. 1995. Hybrid vigor in parasites of interspecific crosses between two mice species. Heredity 74:48-52.
38. Mouse Genome Sequencing Consortium. 2002. Initial sequencing and comparative analysis of the mouse aenome. Nature 420: 520-562.
39. Muller, H. J. 1940. Bearing of the Drosophila work on systematics. Pp. 185-268 in J. S. Huxley, ed. The new systematics. Clarendon Press, Oxford. U.K.
40. _. 1942. Isolating mechanisms, evolution, and temperature. Biol. Symp. 6:71-125.
41. Munclinger, P., E. Bozikova, M. Sugerkova, J. Pialek, and M. Macholan. 2002. Genetic variation in house mice (Mus, Muridae, Rodentia) from the Czech and Slovak Republics. Folia Zool. 51: 81-92.
42. Noor, M. A. F. 2003. Genes to make new species. Nature 423: 699-700.
43. Orr, H. A. 1989. Genetics of sterility in hybrids between two subspecies of Drosophila. Evolution 43:180-189.
44. _. 1995. The population genetics of speciation: the evolution of hybrid incompatibilities. Genetics 139:1805-1813.
45. _. 1996. Dobzhansky, Batcson, and the genetics of speciation. Genetics 144:1331-1335.
46. _. 1997. Haldane's rule. Ann. Rev. Ecol. Syst. 28:195-218.
47. Orr, H. A., and J. A. Coyne. 1989. The genetics of postzygotic isolation in the Drosophila virilis group. Genetics 121:527-537.
48. Pantazidis, A. C., and E. Zouros. 1988. Location of an autosomal factor causing sterility in Drosophila mojavensis males carrying the Drosophila arizonensis Y chromosome. Heredity 60: 299-304.
49. Payseur, B. A., and M. W. Nachman. 2004. The genomics of speciation: investigating the molecular correlates of X chromosome introgression across a hybrid zone between Mus domesticus and Mus musculus. Biol. J. Linn. Soc., In press.
50. Perez, D. E., and C.-I. Wu. 1995. Further characterization of the Odysseus locus of hybrid sterility in Drosophila: one gene is not enough. Genetics 140:201-206.
51. Pialek, J., and N. H. Barton. 1997. The spread of an advantageous allele across a barrier: the effects of random drift and selection against heterozygotes. Genetics 145:493-504.
52. Porter, A. H., R. Wenger, H. Geiger, A. Scholl, and A. M. Shapiro. 1997. The Pontia daplidice-edusa hybrid zone in northwestern Italy. Evolution 51:1561-1573.
53. Presgraves, D. C. 2003. A fine-scale genetic analysis of hybrid incompatibilities in Drosophila. Genetics 163:955-972.
54. Presgraves, D. C., L. Balagopalan, S. M. Abymayr, and H. A. Orr. 2003. Adaptive evolution drives divergence of a hybrid inviability gene between two species of Drosophila. Nature 423: 715-719.
55. Prowell, D. P. 1998. Sex linkage and speciation in Lepidoptera. Pp. 309-319 in D. J. Howard and S. H. Berlocher, eds. Endless forms: species and speciation. Oxford Univ. Press, Oxford, U.K.
56. Rieseberg, L. H., and A. C. Buerkle. 2002. Genetic mapping in hybrid zones. Am. Nat. 159:S37-S50.
57. Rieseberg, L. H., J. Whitton, and K. Gardner. 1999. Hybrid zones and the genetic architecture of a barrier to gene flow between two sunflower species. Genetics 152:713-727.
58. Rieseberg, L. H., O. Raymond, D. M. Rosenthal, Z. Lai, K. Livingstone, T. Nakazato, J. L. Durphy, A. E. Schwarzbach, L. A. Donovan, and C. Lexer. 2003. Major ecological transitions in wild sunflowers facilitated by hybridization. Science 301: 1211-1216.
59. Sage, R. D., D. Heyneman, K.-C. Lim, and A. C. Wilson. 1986. Wormy mice in a hybrid zone. Nature 324:60-63.
60. Sage, R. D., W. R. Atchley, and E. Capanna. 1993. House mice as models in systematic biology. Syst. Biol. 42:523-561.
61. Schnell, G. D., and R. K. Selander. 1981. Environmental and morphological correlates of genetic variation in mammals. Pp. 60-69 in J. Joule and M. H. Smith, eds. Mammalian population genetics. Univ. of Georgia Press, Athens, GA.
62. Selander, R. K., and S. Y. Yang. 1969. Protein polymorphism and genie heterozgyosity in a wild population of the house mouse (Mus musculus). Genetics 63:653-657.
63. She, J. X., F. Bonhomme, P. Boursot, L. Thaler, and F. Catzeflis. 1990. Molecular phylogenies in the genus Mus: comparative analysis of electrophoretic, scnDNA hybridization, and mtDNA RFLP data. Biol. J. Linn. Soc. 41:83-103.
64. Slatkin, M. 1973. Gene flow and selection in a cline. Genetics 75: 733-756.
65. Smadja, C., and G. Ganem. 2002. Subspecies recognition in the house mouse: a study of two populations from the border of a hybrid zone. Behav. Ecol. 13:312-320.
66. Sperling, F. A. H. 1994. Sex-linked genes and species differences in Lepidoptera. Can. Entomol. 126:807-818.
67. Sperling, F. A. H., and J. R. Spence. 1991. Structure of an asymmetric hybrid zone between two water strider species (Hemiptera: Gerridae: Limnoporus). Evolution 45:1370-1383.
68. Storchova, R., S. Gregorova, D. Buckiova, V. Kyselova, P. Divina, and J. Forejt. 2004. Genetic analysis of X-linked hybrid sterility in the house mouse. Mamm. Genome 15:515-524.
69. Szymura, J. M., and N. H. Barton. 1986. Genetic analysis of a hybrid zone between the fire-bellied toads, Bombina bombina and Bombina variegata, near Cracow in southern Poland. Evolution 40: 1141-1159.
70. _, 1991. The genetic structure of the hybrid zone between fire-bellied toads Bombina bombina and B. variegata: comparisons between transects and loci. Evolution 45:237-261.
71. Tao, Y., S. Chen, D. L. Hartl, and C. C. Laurie. 2003. Genetic dissection of hybrid incompatibilities between Drosophila si-mulans and D. mauritiana. I. Differential accumulation of hybrid male sterility effects on the X and autosomes. Genetics 164: 1383-1397.
72. Ting, C. T., S. C. Tsaur, M. L. Wu, and C.-I. Wu. 1998. A rapidly evolving homeobox at the site of a hybrid sterility gene. Science 282:1501-1504.
73. True, J. R., B. S. Weir, and C. C. Laurie. 1996. A genome-wide survey of hybrid incompatibility factors by the introgression of marked segments of Drosophila mauritiana chromosomes into Drosophila simulans. Genetics 142:819-837.
74. Tucker, P. K., R. D. Sage, J. Warner, A. C. Wilson, and E. M. Eicher. 1992. Abrupt cline for sex chromosomes in a hybrid zone between two species of mice. Evolution 46:1146-1163.
75. Turelli, M., and H. A. Orr. 1995. The dominance theory of Haldane's rule. Genetics 140:389-402.
76. _. 2000. Dominance, epistasis and the genetics of postzygotic isolation. Genetics 154:1663-1679.
77. Ursin, E. 1952. Occurrence of voles, mice, and rats (Muridae) in Denmark, with a special note on a zone of intergradation between two subspecies of the house mouse (Mus musculus L.). Vid. Medd. Dansk. Naturhist. Foren, 114:217-244.
78. Vanlerberghe, F., B. Dod, P. Boursot, M. Bellis, and F. Bonhomme. 1986. Absence of Y-chromosome introgression across the hybrid zone between Mus musculus domesticus and Mus musculus musculus. Genet. Res. 48:191-197.
79. Vanlerberghe, F., P. Boursot, J. Catalan, S. Guerasimov, F. Bonhomme, B. Botev, and L. Thaler. 1988. Analyse genetique de la zone d'hybridation entre les deux sous-especes de souris M. m. domesticus et M. m. musculus en Bulgarie. Genome 30: 427-437.
80. Wade, C. M., E. J. Kulbokas, A. W. Kirby, M. C. Zody, J. C. Mullikin, E. S. Lander, K. Lindblad-Toh, and M. J. Daly. 2002. The mosaic structure of variation in the laboratory mouse genome. Nature 420:574-578.
81. Wittbrodt, J., D. Adam, B. Malitschek, W. Mqaueler, F. Raulf, A. Telling, S. M. Robertson, and M. Schartl. 1989. Novel putative receptor tyrosine kinase encoded by the melanoma-inducing Tu locus in Xiphophorus. Nature 341:415-421.
82. Wu, C.-I., and A. T. Beckenbach. 1983. Evidence for extensive genetic differentiation between the sex-ratio and the standard arrangement of Drosophila pseudoobscura and D. persimilis and identification of hybrid sterility factors. Genetics 105:71-86.
83. Yonekawa, H., K. Moriwaki, O. Gotoh, J. Watanabe, J.-I. Hayashi, N. Miyashita, M. L. Petras, and Y. Tagashira. 1980. Relationship between laboratory mice and subspecies Mus musculus domesticus based on restriction endonuclease cleavage patterns of mitochondrial DNA. Jpn. J. Genet. 55:289-296.
84. Zouros, E., K. Lofdahl, and P. A. Martin. 1988. Male hybrid sterility in Drosophila: interactions between autosomes and sex chromosomes in crosses of D. mojavensis and D. arizonensis. Evolution 42:1321-1331.