Asymmetrical reproductive character displacement in the house mouse

Journal of Evolutionary Biology

Volumn 18, Issue 6, 2005, Pages 1485-1493

  Smadja, C ^a,b   Ganem, G ^a  

^a INSTITUT DES SCIENCES DE L EVOLUTION   (France)

^b CENTRE D ECOLOGIE FONCTIONNELLE ET EVOLUTIVE   (France)

Author keywords

Asymmetrical divergence; House mouse; Mate preference; Parapatric hybridization; Premating isolation; Reinforcement; Reproductive character displacement

Indexed keywords

CHARACTER DISPLACEMENT; HYBRIDIZATION; MATE CHOICE; REPRODUCTION; RODENT;

ANALYSIS OF VARIANCE; ANIMAL; ARTICLE; COMPARATIVE STUDY; EUROPE; GENETIC SELECTION; HYBRIDIZATION; MOUSE; PHYSIOLOGY; POPULATION DYNAMICS; POPULATION GENETICS; SEXUAL BEHAVIOR; SPECIES DIFFERENCE;

ANALYSIS OF VARIANCE; ANIMALS; EUROPE; GENETICS, POPULATION; HYBRIDIZATION, GENETIC; MICE; POPULATION DYNAMICS; SELECTION (GENETICS); SEXUAL BEHAVIOR, ANIMAL; SPECIES SPECIFICITY;

MUS MUSCULUS; MUS MUSCULUS DOMESTICUS; MUS MUSCULUS MUSCULUS;

EID: 28444480656     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/j.1420-9101.2005.00944.x     Document Type: Article

References (67)

1. Auffray, J.C., Vanlerberghe, F. & Britton-Davidian, J. 1990. The house mouse progression in Eurasia: a paleontological and archeozoological approach. Biol. J. Lin. Soc. 41: 13-25.
2. Benedix, J.H. & Howard, D.J. 1991. Calling song displacement in a zone of overlap and hybridization. Evolution 45: 1751-1759.
3. Boissinot, S. & Boursot, P. 1997. Discordant phylogeographic patterns between the Y chromosome and mitochondrial DNA in the house mouse: selection on the Y chromosome. Genetics 146: 1019-1034.
4. Bordenstein, S.R., Drapeau, M.D. & Werren, J.H. 2000. Intraspecific variation in sexual isolation in the jewel wasp Nasonia. Evolution 54: 567-573.
5. Boursot, P., Auffray, J.-C., Britton-Davidian, J. & Bonhomme, F. 1993. The evolution of house mice. Ann. Rev. Ecol. Sys. 24: 119-152.
6. Boursot, P., Din, W., Anand, R., Darviche, D., Dod, B., Von Deimling, F., Talwar, G.P. & Bonhomme, F. 1996. Origin and radiation of the house mouse: mitochondrial DNA phylogeny. J. Evol. Biol. 9: 391-415.
7. Britton-Davidian, J., Fel-Clair, F., Lopez, J., Alibert, P. & Boursot, P. 2005. Postzygotic isolation between the two European subspecies of the house mouse: estimates from fertility patterns in wild and laboratory-bred hybrids. Biol. J. Linn. Soc. 84: 379-393.
8. Butlin, R. 1989. Reinforcement of premating isolation. In: Speciation and its Consequences (D. Otte & J. A. Endler, eds), pp. 158-179. Sinauer Associates Inc., Sunderland, MA, USA.
9. Butlin, R. 1994. Genetic variation in mating signals and responses. In: Speciation and the Recognition Concept (D. M. Lambert & H. G. Spencer, eds), pp. 327-366. Johns Hopkins University Press, Baltimore, London.
10. Butlin, R.K. 1995. Reinforcement: an idea evolving. Trends Ecol. Evol. 10: 432-434.
11. Butlin, R.K. & Ritchie, M.G. 1991. Variation in female mate preference across a grasshopper hybrid zone. J. Evol. Biol. 4: 227-240.
12. Cain, M.L., Andreasen, V. & Howard, D.J. 1999. Reinforcing selection is effective under a relatively broad set of conditions in a mosaic hybrid zone. Evolution 53: 1343-1353.
13. Coyne, J.A. & Orr, H.A. 1989. Patterns of speciation in Drosophila. Evolution 43: 362-381.
14. Dempster, E.R., Dempster, R. & Perrin, M.R. 1993. Behavioural divergence in allopatric and sympatric Gerbil species (Rodentia: Gerbillinae). Ethology 93: 300-314.
15. Dobzhansky, T. 1940. Speciation as a stage in evolutionary divergence. Am. Nat. 74: 312-321.
16. Dod, B., Jermiin, L.S., Boursot, P., Chapman, V.H., Nielsen, J.T. & Bonhomme, F. 1993. Counter-selection on sex chromosomes in the Mus musculus European hybrid zone. J. Evol. Biol. 6: 529-546.
17. Dod, B., Smadja, C., Karn, R.C. & Boursot, P. 2005. Testing for selection on the Androgen-Binding-Protein in the Danish house mouse hybrid zone. Biol. J. Linn. Soc. 84: 447-459.
18. Endler, J.A. & Houde, A.E. 1995. Geographic variation in female preference for male traits in Poecilia reticulata. Evolution 49: 456-468.
19. Fel-Clair, P., Lenormand, T., Catalan, J., Grobert, J., Orth, A., Boursot, P., Viroux, M.-C. & Britton-Davidian, J. 1996. Genomic incompatibilities in the hybrid zone between house mice in Denmark: evidence from steep and non-coincident chromosomal clines for Robertsonian fusions. Genet. Res. Camb. 67: 123-134.
20. Ferreira, M.H. & Ferguson, J.W. 2002. Geographic variation in the calling song of the field cricket Gryllus bimaculatus (Orthoptera: Gryllidae) and its relevance to mate recognition and mate choice. J. Zool. Lond. 257: 163-170.
21. Ferris, S.D., Sage, R.D., Huang, C.M., Nielsen, J.T., Ritte, U. & Wilson, A.C. 1983. Flow of mitochondrial DNA across a species boundary. Proc. Nat. Acad. Sci. USA 80: 2290-2294.
22. Forejt, J. 1996. Hybrid sterility in the mouse. Trends Genet. 12: 412-417.
23. Foster, S.A. 1999. The geography of behavior: an evolutionary perspective. Trends Ecol. Evol 14: 190-195.
24. Gabor, C.R. & Ryan, M.J. 2001. Geographical variation in reproductive character displacement in mate choice by male sailfin mollies. Proc. R. Soc. Lond. B 268: 1063-1070.
25. Geyer, L.B. & Palumbi, S.R. 2003. Reproductive character displacement and the genetics of gamete recognition in tropical sea urchins. Evolution 57: 1049-1060.
26. Higashi, M., Takimoto, G. & Yamamura, N. 1999. Sympatric speciation by sexual selection. Nature 402: 523-526.
27. Higgle, M., Chenoweth, S. & Blows, M.W. 2000. Natural selection and the reinforcement of mate recognition. Science 290: 519-521.
28. Hobel, G. & Gerhardt, H.C. 2003. Reproductive character displacement in the acoustic communication system of green tree frogs (Hyla cinerea). Evolution 57: 894-904.
29. Howard, D.J. 1993. Reinforcement: origin, dynamics, and fate of an evolutionary hypothesis. In: Hybrid Zones and the Evolutionary Process (R. G. Harrison, ed.), pp. 46-69. Oxford University Press, New York.
30. Howard, D.J. & Gregory, P.G. 1993. Post-insemination signalling systems and reinforcement. Philos. Trans. Roy. Soc. Lond. B 340: 231-236.
31. Jiggins, C.D. & Mallet, J. 2000. Bimodal hybrid zones and speciation. Trends Ecol. Evol. 15: 250-255.
32. Kawata, M. & Yoshimura, J. 2000. Speciation by sexual selection in hybridizing populations without viability selection. Evol. Ecol. Res. 2: 897-909.
33. Kawecki, T. 1996. Sympatric speciation driven by beneficial mutations. Proc. Roy. Soc. Lond. B 263: 1515-1520.
34. Kawecki, T. 1997. Sympatric speciation via habitat specialization driven by deleterous mutations. Evolution 51: 1751-1763.
35. Lemmon, A.R., Smadja, C. & Kirkpatrick, M. 2004. Reproductive character displacement is not the only possible outcome of reinforcement. J. Evol. Biol. 17: 177-183.
36. Liou, L.W. & Price, T.D. 1994. Speciation by reinforcement of premating isolation. Evolution 48: 1451-1459.
37. Marshall, D.C. & Cooley, J.R. 2000. Reproductive character displacement and speciation in periodical cicadas, with description of a new species, 13-year Magicicada neotredecim. Evolution 54: 1313-1325.
38. McElfresh, J.S. & Millar, J.G. 1999. Geographic variation in sex pheromone blend of Hemileuca electra from Southern California. J. Chem. Ecol. 25: 2505-2525.
39. Moulia, C., Aussel, J.P., Bonhomme, F., Boursot, P., Nielsen, J.T. & Renaud, F. 1991. Wormy mice in a hybrid zone: a genetic control of susceptibility to parasite infection. J. Evol. Biol. 4: 679-687.
40. Moulia, C., Le Brun, N., Dallas, J., Orth, A. & Renaud, F. 1993. Experimental evidence of genetic determinism in high susceptibility to intestinal pin worms infection in mice: a hybrid zone model. Parasitology 106: 387-393.
41. Noor, M.A. 1995. Speciation driven by natural selection in Drosophila. Nature 375: 674-675.
42. Noor, M.A.F. 1999. Reinforcement and other consequences of sympatry. Heredity 83: 503-508.
43. Nosil, P., Crespi, B.J. & Sandoval, C.P. 2003. Reproductive isolation driven by the combined effects of ecological adaptation and reinforcement. Proc. Roy. Soc. Lond. B 270: 1911-1918.
44. Pfennig, K.S., Rapa, K. & McNatt, R. 2000. Evolution of male mating behavior: male spadefoot toads preferentially associate with conspecific males. Behav. Ecol. Sociobiol. 48: 69-74.
45. Pfennig, K.S. & Simovich, M.A. 2002. Differential selection to avoid hybridization in two toads species. Evolution 56: 1840-1848.
46. Raufaste, N., Orth, A., Belkhir, K., Senet, D., Smadja, C., Baird, S.J.E., Bonhomme, F., Dod, B. & Boursot, P. 2005. Inference of selection and migration in the Danish house mouse hybrid zone. Biol. J. Linn. Soc. 84: 593-616.
47. Rice, W.R. 1989. Analysing tables of statistical tests. Evolution 43: 223-225.
48. Ritchie, M.G., Butlin, R.K. & Hewitt, G.M. 1992. Fitness consequences of potential assortative mating inside and outside a hybrid zone in Chorthippus parallelus (Orthoptera: Acrididae): implications for reinforcement and sexual selection theory. Biol. J. Linn. Soc. 45: 219-234.
49. Rundle, H.D. & Schluter, D. 1998. Reinforcement of stickleback mate preferences: sympatry breeds contempt. Evolution 52: 200-208.
50. Sadedin, S. & Littlejohn, M.J. 2003. A spatially explicit individual-based model of reinforcement in hybrid zones. Evolution 57: 962-970.
51. Saetre, G.-P., Moum, T., Bures, S., Kral, M., Adamjan, M. & Moreno, J. 1997. A sexually selected character displacement in flycatchers reinforces premating isolation. Nature 387: 589-592.
52. Sage, R.D. 1981. Wild mice. In: The Mouse in Biomedical Research (H. L. e. a. Foster, ed.), pp. 39-90. Academic press, New York.
53. Sage, R.D., Heyneman, D., Lim, K.-C. & Wilson, A.C. 1986. Wormy mice in a hybrid zone. Nature 324: 60-63.
54. Sanderson, N. 1989. Can gene flow prevent reinforcement? Evolution 43: 1223-1235.
55. Sanderson, N., Szymura, J.M. & Barton, N.H. 1992. Variation in mating call across the hybrid zone between the fire-bellied toads Bombina bombina and B. varietaga. Evolution 46: 595-607.
56. SAS Institute. 1989. SAS/STAT. User's Guide. Version 6, 4th edn. SAS Institute Inc., Cary, NC, USA.
57. Servedio, M.R. & Kirkpatrick, M. 1997. The effects of gene flow on reinforcement. Evolution 51: 1764-1772.
58. Smadja, C. & Ganem, G. 2002. Subspecies recognition in the house mouse: a study of two populations from the border of a hybrid zone. Behav. Ecol. 13: 312-320.
59. Smadja, C., Catalan, J. & Ganem, G. 2004. Strong premating divergence in a unimodal hybrid zone between two subspecies of the house mouse. J. Evol. Biol. 17: 165-176.
60. Smith, M.H. 1965. Behavioral discrimination shown by allopatric and sympatric males of Peromyscus eremicus and Peromyscus californicus between females of the same two species. Evolution 19: 430-435.
61. Sokal, R.R. & Rohlf, F.J. 1981. Biometry. The Principles and Practices of Statistics in Biological Research, 2nd edn. Freeman, W. H. and Company, New York.
62. Thuesen, P. 1977. A comparison of the agonistic behaviour of the Mus musculus L. and Mus musculus domesticus Rutty (Mammalia and Rodentia). Vidensk. Dan. Naturhist. Foren. 140: 117-128.
63. Turner, G.F. & Burrows, M.T. 1995. A model of sympatric speciation by sexual selection. Proc. R. Soc. Lond. B 260: 287-292.
64. Tynkkynen, K., Rantala, M.J. & Suhonen, J. 2004. Interspecific aggression and character displacement in the damselfly Calopteryx splendens. J. Evol. Biol. 17: 759-767.
65. Van Zegeren, K. & Van Oortmerssen, G.A. 1981. Frontier disputes between the West and East-European house mouse in Schleswig-Holstein, West Germany. Z. Säugetierkunde 46: 363-369.
66. Vanlerberghe, F., Dod, B., Boursot, P., Bellis, M. & Bonhomme, F. 1986. Absence of Y-chromosome introgression across the hybrid zone between Mus musculus domesticus and Mus musculus musculus. Genet. Res. Camb. 48: 191-197.
67. Zar, J.H. 1999. Biostatistical Analysis, 4th edn. Upper Saddle River, Prentice Hall.