Faster fertilization rate in conspecific versus heterospecific matings in house mice

Evolution

Volumn 63, Issue 1, 2009, Pages 20-28

  Dean, Matthew D ^a   Nachman, Michael W ^a  

^a University of Arizona   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CONSPECIFIC; FERTILIZATION (REPRODUCTION); GENE FLOW; HYBRIDIZATION; LABORATORY METHOD; PHENOTYPE; REPRODUCTIVE ISOLATION; REPRODUCTIVE STRATEGY; RODENT; SPERM COMPETITION;

ANIMAL; ARTICLE; CROSS BREEDING; FEMALE; FERTILIZATION; MALE; MOUSE; MOUSE STRAIN; PHYSIOLOGY; SPECIES DIFFERENCE; SPERMATOZOON;

ANIMALS; CROSSES, GENETIC; FEMALE; FERTILIZATION; MALE; MICE; MICE, INBRED STRAINS; SPECIES SPECIFICITY; SPERMATOZOA;

MUS MUSCULUS; MUS MUSCULUS DOMESTICUS;

EID: 58249139998     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2008.00499.x     Document Type: Article

References (90)

1. Agrawal, Y., and T. Vanha-Perttula. 1987. Effect of secretory particles in bovine seminal vesicle secretion on sperm motility and acrosome reaction. J. Reprod. Fertil. 79 : 409 419.
2. Anderson, D. J., and T. H. Tarter. 1982. Immunosuppressive effects of mouse seminal plasma components in vivo and in vitro. J. Immunol. 128 : 535 539.
3. Auffray, J. C., F. Vanlerberghe, and J. Britton-Davidian. 1990. The house mouse progression in Eurasia: a paleontological and archeozoological approach. Biol. J. Linn. Soc. 41 : 13 25.
4. Birkhead, T. R., and T. Pizzari. 2002. Postcopulatory sexual selection. Nat. Rev. Genet. 3 : 262 273.
5. Birkhead, T. R., and J. P. Brillard. 2007. Reproductive isolation in birds: postcopulatory prezygotic barriers. Trends Ecol. Evol. 22 : 266 272.
6. Boursot, P., J.-C. Auffray, J. Britton-Davidian, and F. Bonhomme. 1993. The evolution of house mice. Annu. Rev. Ecol. Syst. 24 : 119 152.
7. Carballada, R., and P. Esponda. 1997. Fate and distribution of seminal plasma proteins in the genital tract of the female rat after natural mating. J. Reprod. Fertil. 109 : 325 335.
8. Carballada, R., and P. Esponda. 1998. Binding of seminal vesicle proteins to the plasma membrane of rat spermatozoa in vivo and in vitro. Int. J. Androl. 21 : 19 28.
9. Carballada, R., and P. Esponda. 1999. Effect of antibodies against seminal vesicle secretion on fertility in the rat. Zygote 7 : 223 231.
10. Castillo-Davis, C. I., F. A. Kondrashov, D. L. Hartl, and R. J. Kulathinal. 2004. The functional genomic distribution of protein divergence in two animal phyla: coevolution, genomic conflict, and constraint. Genome Res. 14 : 802 811.
11. Chang, A. S. 2004. Conspecific sperm precedence in sister species of Drosophila with overlapping ranges. Evolution 58 : 781 789.
12. Clark, A. G., and D. J. Begun. 1998. Female genotypes affect sperm displacement in Drosophila. Genetics 149 : 1487 1493.
13. Clark, A. G., D. J. Begun, and T. Prout. 1999. Female × male interactions in Drosophila sperm competition. Science 283 : 217 220.
14. Clark, A. G., E. T. Dermitzakis, and A. Civetta. 2000. Nontransitivity of sperm precedence in Drosophila. Evolution 54 : 1030 1035.
15. Clark, N. L., J. E. Aagaard, and W. J. Swanson. 2006. Evolution of reproductive proteins from animals and plants. Reprod. Fertil. Dev. 131 : 11 22.
16. Coyne, J. A., and H. A. Orr. 2004. Speciation. Sinauer Associates, Inc., Sunderland, Massachusetts.
17. Dean, M. D., K. G. Ardlie, and M. W. Nachman. 2006. The frequency of multiple paternity suggests that sperm competition is common in house mice (Mus domesticus). Mol. Ecol. 15 : 4141 4151.
18. Dean, M. D., J. M. Good, and M. W. Nachman. 2008. Adaptive evolution of proteins secreted during sperm maturation: an analysis of the mouse epididymal transcriptome. Mol. Biol. Evol. 25 : 383 392.
19. Dixon, S. M., J. A. Coyne, and M. A. Noor. 2003. The evolution of conspecific sperm precedence in Drosophila. Mol. Ecol. 12 : 1179 1184.
20. Dod, B., L. S. Jermiin, P. Boursot, V. H. Chapman, J. T. Nielsen, and F. Bonhomme. 1993. Counterselection on sex chromosomes in the Mus musculus European hybrid zone. J. Evol. Biol. 6 : 529 546.
21. Dorus, S., P. D. Evans, G. J. Wyckoff, S. S. Choi, and B. T. Lahn. 2004. Rate of molecular evolution of the seminal protein gene SEMG2 correlates with levels of female promiscuity. Nat. Genet. 36 : 1326 1329.
22. Fricke, C., and G. Arnqvist. 2004. Conspecific sperm precedence in flour beetles. Anim. Behav. 67 : 729 732.
23. Fukuda, Y., M. B. Maddock, and M. C. Chang. 1979. In vitro fertilization of two species of deer mouse eggs by homologous or heterologous sperm and penetration of laboratory mouse eggs by deer mouse sperm. J. Exp. Zool. 207 : 481 489.
24. Ganem, G., C. Ginane, M.-F. Ostrowski, and A. Orth. 2005. Assessment of mate preference in the house mouse with reference to investigations on assortative mating. Biol. J. Linn. Soc. 84 : 461 471.
25. Georgiou, A. S., E. Sostaric, C. H. Wong, A. P. Snijders, P. C. Wright, H. D. Moore, and A. Fazeli. 2005. Gametes alter the oviductal secretory proteome. Mol. Cell. Proteomics. 4 : 1785 1796.
26. Gibbs, R. A., G. M. Weinstock, M. L. Metzker, D. M. Muzny, E. J. Sodergren, S. Scherer, G. Scott, D. Steffen, K. C. Worley, P. E. Burch, et al. 2004. Genome sequence of the Brown Norway rat yields insights into mammalian evolution. Nature 428 : 493 521.
27. Ginsberg, J. R., and U. W. Huck. 1989. Sperm competition in mammals. Trends Ecol. Evol. 4 : 74 79.
28. Good, J. M., M. A. Handel, and M. W. Nachman. 2007. Asymmetry and polymorphism of hybrid male sterility during the early stages of speciation in house mice. Evolution 62 : 50 65.
29. Gray, A. P. 1958. Bird hybrids: a check list with bibliography. Tech. Comm. 13 of Commonwealth Bureau Anim. Breed. Genet. Commonwealth Agricultural Bureau, Bucks, U. K.
30. Gray, A. P. 1972. Mammalian hybrids-a check-list with bibliography. Commonwealth Agricultural Bureaux, Bucks, England.
31. Gregory, P. G., and D. J. Howard. 1994. A postinsemination barrier to fertilization isolates two closely related ground crickets. Evolution 48 : 705 710.
32. Hanada, A., and M. C. Chang. 1972. Penetration of zona-free eggs by spermatozoa of different species. Biol. Reprod. 6 : 300 309.
33. Harshman, L. G., and T. Prout. 1994. Sperm displacement without sperm transfer in Drosophila melanogaster. Evolution 48 : 758 766.
34. Henault, M. A., and G. J. Killian. 1996. Effect of homologous and heterologous seminal plasma on the fertilizing ability of ejaculated bull spermatozoa assessed by penetration of zona-free bovine oocytes. J. Reprod. Fertil. 108 : 199 204.
35. Henault, M. A., G. J. Killian, J. F. Kavanaugh, and L. C. Griel, Jr. 1995. Effect of accessory sex gland fluid from bulls of differing fertilities on the ability of cauda epididymal sperm to penetrate zona-free bovine oocytes. Biol. Reprod. 52 : 390 397.
36. Hewitt, G. M., P. Mason, and R. A. Nichols. 1989. Sperm precedence and homogamy across a hybrid zone in the alpine grasshopper Podisma pedestris. Heredity 62 : 343 354.
37. Howard, D. J. 1999. Conspecific sperm and pollen precedence and speciation. Annu. Rev. Ecol. Syst. 30 : 109 132.
38. Howard, D. J., P. G. Gregory, J. Chu, and M. L. Cain. 1998. Conspecific sperm precedence is an effective barrier to hybridization between closely related species. Evolution 52 : 511 516.
39. Huang, Y. H., S. T. Chu, and Y. H. Chen. 2000. A seminal vesicle autoantigen of mouse is able to suppress sperm capacitation-related events stimulated by serum albumin. Biol. Reprod. 63 : 1562 1566.
40. Irwin, M., N. Nicholson, J. T. Haywood, and G. R. Poirier. 1983. Immunofluorescent localization of a murine seminal vesicle proteinase inhibitor. Biol. Reprod. 28 : 1201 1206.
41. Jansa, S. A., B. L. Lundrigan, and P. K. Tucker. 2003. Tests for positive selection on immune and reproductive genes in closely related species of the murine genus Mus. J. Mol. Evol. 56 : 294 307.
42. Kawano, N., and M. Yoshida. 2007. Semen-coagulating protein, SVS2, in mouse seminal plasma controls sperm fertility. Biol. Reprod. 76 : 353 361.
43. Kelleher, E. S., W. J. Swanson, and T. A. Markow. 2007. Gene duplication and adaptive evolution of digestive proteases in Drosophila arizonae female reproductive tracts. PLoS Genet. 3 : e148.
44. Knowles, L. L., and T. A. Markow. 2001. Sexually antagonistic coevolution of a postmating-prezygotic reproductive character in desert Drosophila. Proc. Natl. Acad. Sci. USA 98 : 8692 8696.
45. Kochhar, H. P., K. B. Rao, A. M. Luciano, S. M. Totey, F. Gandolfi, P. K. Basrur, and W. A. King. 2002. In vitro production of cattle-water buffalo (Bos taurus - Bubalus bubalis) hybrid embryos. Zygote 10 : 155 162.
46. Kouba, A. J., M. W. Atkinson, A. R. Gandolf, and T. L. Roth. 2001. Species-specific sperm-egg interaction affects the utility of a heterologous bovine in vitro fertilization system for evaluating antelope sperm. Biol. Reprod. 65 : 1246 1251.
47. Lambert, H. 1984. Role of sperm-surface glycoproteins in gamete recognition in two mouse species. J. Reprod. Fertil. 70 : 281 284.
48. Lopyrin, A. I., and N. V. Loginova. 1963. Remote hybridization of animals. Anim. Br. Abstr. 22 : 227.
49. Macholán, M., P. Munclinger, M. Šugerková, P. Dufková, B. Bímová, E. Božíková, J. Zima, and J. Piálek. 2007. Genetic analysis of autosomal and X-linked markers across a mouse hybrid zone. Evolution 61 : 746 771.
50. Maddock, M. B., and W. D. Dawson. 1974. Artificial insemination of deermice (Peromyscus maniculatus) with sperm from other rodent species. J. Embryol. Exp. Morph. 31 : 621 634.
51. Munclinger, P., E. Božíková, M. Š ugerková, J. Piálek, and M. Macholán. 2002. Genetic variation in house mice (Mus, Muridae, Rodentia) from the Czech and Slovak Republics. Folia. Zool. 51 : 81 92.
52. Nagy, A., M. Gertsenstein, K. Vintersten, and R. Behringer. 2003. Manipulating the mouse embryo. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
53. Nielsen, R., C. Bustamante, A. G. Clark, S. Glanowski, T. B. Sackton, M. J. Hubisz, A. Fledel-Alon, D. M. Tanenbaum, D. Civello, T. J. White, et al. 2005. A scan for positively selected genes in the genomes of humans and chimpanzees. PLoS Biol. 3 : e170.
54. O, W. S., H. Q. Chen, and P. H. Chow. 1988. Effects of male accessory sex gland secretions on early embryonic development in the golden hamster. J. Reprod. Fertil. 84 : 341 344.
55. Pang, S. F., P. H. Chow, and T. M. Wong. 1979. The role of the seminal vesicles, coagulating glands and prostate glands on the fertility and fecundity of mice. J. Reprod. Fertil. 56 : 129 132.
56. Payseur, B. A., J. G. Krenz, and M. W. Nachman. 2004. Differential patterns of introgression across the X chromosome in a hybrid zone between two species of house mice. Evolution 58 : 2064 2078.
57. Peitz, B. 1988. Effects of seminal vesicle fluid components on sperm motility in the house mouse. J. Reprod. Fertil. 83 : 169 176.
58. Peitz, B., and D. Bennett. 1981. Inhibition of complement-mediated cytotoxicity of antisera by fluid secreted by the seminal vesicle of the house mouse. J. Reprod. Immunol. 3 : 109 116.
59. Peitz, B., and P. Olds-Clarke. 1986. Effects of seminal vesicle removal on fertility and uterine sperm motility in the house mouse. Biol. Reprod. 35 : 608 617.
60. Price, C. S. 1997. Conspecific sperm precedence in Drosophila. Nature 388 : 663 666.
61. Price, C. S., C. H. Kim, C. J. Gronlund, and J. A. Coyne. 2001. Cryptic reproductive isolation in the Drosophila simulans species complex. Evolution 55 : 81 92.
62. Queen, K., C. B. Dhabuwala, and C. G. Pierrepoint. 1981. The effect of the removal of the various accessory sex glands on the fertility of male rats. J. Reprod. Fertil. 62 : 423 426.
63. Ramm, S. A., and P. Stockley. 2007. Ejaculate allocation under varying sperm competition risk in the house mouse, Mus musculus domesticus. Behav. Ecol. 18 : 491 495.
64. Robinson, R., R. Richardson, K. Hinds, D. Clayton, and G. R. Poirier. 1987. Features of a seminal proteinase inhibitor- zona pellucida-binding component on murine spermatozoa. Gamete Res. 16 : 217 228.
65. Robinson, T., N. A. Johnson, and M. J. Wade. 1994. Postcopulatory, prezygotic isolation: intraspecific and interspecific sperm precedence in Tribolium spp., flour beetles. Heredity 73 : 155 159.
66. Roldan, E. R., and R. Yanagimachi. 1989. Cross-fertilization between Syrian and Chinese hamsters. J. Exp. Zool. 250 : 321 328.
67. Roldan, E. R., A. D. Vitullo, M. S. Merani, and I. Von Lawzewitsch. 1985. Cross fertilization in vivo and in vitro between three species of vesper mice, Calomys (Rodentia, Cricetidae). J. Exp. Zool. 233 : 433 442.
68. Rugman-Jones, P. F., and P. E. Eady. 2007. Conspecific sperm precedence in Callosobruchus subinnotatus (Coleoptera: Bruchidae): mechanisms and consequences. Proc. R. Soc. Lond. B. 274 : 983 988.
69. Salcedo, T., A. Geraldes, and M. W. Nachman. 2007. Nucleotide variation in wild and inbred mice. Genetics 177 : 2277 2291.
70. 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.
71. Slavík, T., V. Kopečný, and J. Fulka. 1997. Developmental failure of hybrid embryos originated after fertilization of bovine oocytes with ram spermatozoa. Mol. Reprod. Dev. 48 : 344 349.
72. 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.
73. Smadja, C., and G. Ganem. 2005. Asymmetrical reproductive character displacement in the house mouse. J. Evol. Biol. 18 : 1485 1493.
74. Smadja, G., J. Catalan, and C. Ganem. 2004. Strong premating divergence in a unimodal hybrid zone between two subspecies of the house mouse. J. Evol. Biol. 17 : 165 176.
75. Snyder, R. L. 1967. Fertility and reproductive performance of grouped male mice. Pp. 458 472 in K. Benirschke, ed. Comparative aspects of reproductive failure. Springer-Verlag, New York.
76. Stauss, C. R., T. J. Votta, and S. S. Suarez. 1995. Sperm motility hyperactivation facilitates penetration of the hamster zona pellucida. Biol. Reprod. 53 : 1280 1285.
77. Suarez, S. S., and H. C. Ho. 2003. Hyperactivation of mammalian sperm. Cell. Mol. Biol. 49 : 351 356.
78. Sutovsky, P., T. C. McCauley, M. Sutovsky, and B. N. Day. 2003. Early degradation of paternal mitochondria in domestic pig (Sus scrofa) is prevented by selective proteasomal inhibitors lactacystin and MG132. Biol. Reprod. 68 : 1793 1800.
79. Suzuki, H., T. Shimada, M. Terashima, K. Tsuchiya, and K. Aplin. 2004. Temporal, spatial, and ecological modes of evolution of Eurasian Mus based on mitochondrial and nuclear gene sequences. Mol. Phylogenet. Evol. 33 : 626 646.
80. Swanson, W. J., and V. D. Vacquier. 2002. The rapid evolution of reproductive proteins. Nat. Rev. Genet. 3 : 137 144.
81. Swanson, W. J., R. Nielsen, and Q. Yang. 2003. Pervasive adaptive evolution in mammalian fertilization proteins. Mol. Biol. Evol. 20 : 18 20.
82. Teeter, K. C., B. A. Payseur, L. W. Harris, M. A. Bakewell, L. M. Thibodeau, J. E. O'Brien, J. G. Krenz, M. A. Sans-Fuentes, M. W. Nachman, and P. K. Tucker. 2007. Genome-wide patterns of gene flow across a house mouse hybrid zone. Genome Res. 18 : 67 76.
83. Thaler, C. J. 1989. Immunological role for seminal plasma in insemination and pregnancy. Am. J. Reprod. Immunol. 21 : 147 150.
84. Torgerson, D. G., R. J. Kulathinal, and R. S. Singh. 2002. Mammalian sperm proteins are rapidly evolving: evidence of positive selection in functionally diverse genes. Mol. Biol. Evol. 19 : 1973 1980.
85. Turner, L. M., and H. E. Hoekstra. 2006. Adaptive evolution of fertilization proteins within a genus: variation in ZP2 and ZP3 in deer mice (Peromyscus). Mol. Biol. Evol. 23 : 1656 1669.
86. Wade, M. J., H. Patterson, N. W. Chang, and N. A. Johnson. 1994. Postcopulatory, prezygotic isolation in flour beetles. Heredity 72 : 163 167.
87. Waterston, R. H., K. Lindblad-Toh, E. Birney, J. Rogers, J. F. Abril, P. Agarwal, R. Agarwala, R. Ainscough, M. Alexandersson, P. An, et al. 2002. Initial sequencing and comparative analysis of the mouse genome. Nature 420 : 520 562.
88. West, J. D., W. I. Frels, V. E. Papaioannou, J. P. Karr, and V. M. Chapman. 1977. Development of interspecific hybrids of Mus. J. Embryol. Exp. Morphol. 41 : 233 243.
89. Wyckoff, G. J., W. Wang, and C. I. Wu. 2000. Rapid evolution of male reproductive genes in the descent of man. Nature 403 : 304 309.
90. Yanagimachi, R. 1969. In vitro capacitation of hamster spermatozoa by follicular fluid. J. Reprod. Fertil. 18 : 275 286.