Sperm-related phenotypes implicated in both maintenance and breakdown of a natural species barrier in the house mouse

Proceedings of the Royal Society B: Biological Sciences

Volumn 279, Issue 1748, 2012, Pages 4803-4810

  Albrechtová, Jana ^a,b   Albrecht, Tomáš ^a,b   Baird, Stuart J E ^c   Macholán, Miloš ^d   Rudolfsen, Geir ^e   Munclinger, Pavel ^b   Tucker, Priscilla K ^f   Piálek, Jaroslav ^a  

^a INSTITUTE OF VERTEBRATE BIOLOGY   (Czech Republic)

^b CHARLES UNIVERSITY   (Czech Republic)

^c CENTRO DE INVESTIGAÇÃO EM BIODIVERSIDADE E RECURSOS GENÉTICOS   (Portugal)

^d INSTITUTE OF ANIMAL PHYSIOLOGY AND GENETICS   (Czech Republic)

^e NORWEGIAN RADIATION PROTECTION AUTHORITY   (Norway)

^f UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Hybrid zone; Male fitness; Species barrier; Sperm; Y introgression

Indexed keywords

EID: 84868122893     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2012.1802     Document Type: Article

References (65)

1. Abbot, R. et al. In press. Hybridization and speciation. J. Evol. Biol. (doi:10.1111/j.1420-9101.2012.02599.x)
2. Coyne, J. A. & Orr, H. A. 2004 Speciation. Sunderland, MA: Sinauer Associates.
3. Tucker, P. K., Sage, R. D., Warner, J., Wilson, A. C. & Eicher, E. M. 1992 Abrupt cline for sex chromosomes in a hybrid zone between two species of mice. Evolution 46, 1146-1163. (doi:10.2307/2409762)
4. Dod, B., Jermiin, L. S., Boursot, P., Chapman, V. H., Nielsen, J. T. & Bonhomme, F. 1993 Counterselection on sex chromosomes in the Mus musculus European hybrid zone. J. Evol. Biol. 6, 529-546. (doi:10.1046/j.1420-9101.1993.6040529.x)
5. Macholán, M., Munclinger, P., Šugerková, M., Dufková, P., Bi{dotless}́mová, B., Boži{dotless}́ková, E., Zima, J. & Piálek, J. 2007 Genetic analysis of autosomal and X-linked markers across a mouse hybrid zone. Evolution 61, 746-771. (doi:10.1111/j.1558-5646.2007.00065.x)
6. Macholán, M., Baird, S. J. E., Munclinger, P., Dufková, P., Bi{dotless}́mová, B. & Piálek, J. 2008 Genetic conflict outweighs heterogametic incompatibility in the mouse hybrid zone? BMC Evol. Biol. 8, 271-284. (doi:10.1186/1471-2148-8-271)
7. Macholán, M., Baird, S. J. E., Dufková, P., Munclinger, P., Vošlajerová Bi{dotless}́mová, B. & Piálek, J. 2011 Assessing multilocus introgression patterns: a case study on the mouse X chromosome in Central Europe. Evolution 65, 1428-1446. (doi:10.1111/j.1558-5646.2011.01228.x)
8. Teeter, K. C. et al. 2008 Genome-wide patterns of gene flow across a house mouse hybrid zone. Genome Res. 18, 67-76. (doi:10.1101/gr.6757907)
9. Teeter, K. C., Thibodeau, L. M., Gompert, Z., Buerkle, C. A., Nachman, M. W. & Tucker, P. K. 2010 The variable genomic architecture of isolation between hybridizing species of house mice. Evolution 64, 472-485. (doi:10.1111/j.1558-5646.2009.00846.x)
10. Wang, L. et al. 2011 Measures of linkage disequilibrium among neighboring SNPs indicate asymmetries across the house mouse hybrid zone. Mol. Ecol. 20, 2985-3000. (doi:10.1111/j.1365-294X.2011.05148.x)
11. Boursot, P., Auffrey, J. C., Britton-Davidian, J. & Bonhomme, F. 1993 The evolution of house mice. Annu. Rev. Ecol. Syst. 24, 119-152. (doi:10.1146/annurev.ecolsys.24.1.119)
12. Jones, E. P., Van Der Kooij, J., Solheim, R. & Searle, J. B. 2010 Norwegian house mice (Mus musculus musculus/domesticus): distributions, routes of colonization and patterns of hybridization. Mol. Ecol. 19, 5252-5264. (doi:10.1111/j.1365-294X.2010.04874.x)
13. Payseur, B. A., Krenz, J. G. & Nachman, M. W. 2004 Differential patterns of introgression across the X chromosome in a hybrid zone between two species of house mouse. Evolution 58, 2064-2078. (doi:10.1554/03-738)
14. Dufková, P., Macholán, M. & Piálek, J. 2011 Inference of selection and stochastic effects in the house mouse hybrid zone. Evolution 65, 993-1010. (doi:10.1111/j.1558-5646.2011.01222.x)
15. Turner, L. M., Schwahn, D. J. & Harr, B. 2012 Reduced male fertility in common but highly variable in form and severity in a natural house mouse hybrid zone. Evolution 66, 443-458. (doi:10.1111/j.1558-5646.2011.01445.x)
16. Dobzhansky, T. 1936 Studies on hybrid sterility. II. Localization of sterility factors in Drosophila pseudoobscura hybrids. Genetics 21, 113-135.
17. Muller, H. J. 1942 Isolating mechanisms, evolution, and temperature. Biol. Symp. 6, 71-125.
18. Fisher, R. A. 1954 A fuller theory of 'junctions' in inbreeding. Heredity 8, 187-197. (doi:10.1038/hdy.1954.17)
19. Baird, S. J. E. 2006 Fisher's markers of admixture. Heredity 97, 81-83. (doi:10.1038/sj.hdy.6800850)
20. Hewitt, G. M. 1988 Hybrid zones-natural laboratories for evolutionary studies. Trends Ecol. Evol. 3, 158-167. (doi:10.1016/0169-5347(88)90033-X)
21. Vošlajerová Bi{dotless}́mová, B. et al. 2011 Reinforcement selection acting on the European house mouse hybrid zone. Mol. Ecol. 20, 2403-2424. (doi:10.1111/j.1365-294X.2011.05106.x)
22. Baird, S. J. E., Ribas, A., Macholán, M., Albrecht, T., Piálek, J. & Goüy de Bellocq, J. 2012 Where are the wormy mice? A re-examination of hybrid parasitism in the European house mouse hybrid zone. Evolution 66, 2757-2772. (doi:10.1111/j.1558-5646.2012.01633.x)
23. Sage, R. D., Heyneman, D., Lim, K. C. & Wilson, A. C. 1986 Wormy mice in a hybrid zone. Nature 324, 60-62. (doi:10.1038/324060a0)
24. Moulia, C., Aussel, J. P., Bonhomme, F., Boursot, P., Nielsen, J. T. & Renaud, D. 1991 Wormy mice in a hybrid zone: a genetic control of susceptibility to parasite infection. J. Evol. Biol. 4, 679-687. (doi:10.1046/j.1420-9101.1991.4040679.x)
25. 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. (doi:10.1111/j.1095-8312.2005.00441.x)
26. Alibert, P., Fel-Clair, F., Manolakou, K., Britton-Davidian, J. & Auffray, J. C. 1997 Developmental stability, fitness, and trait size in laboratory hybrids between European subspecies of the house mouse. Evolution 51, 1284-1295. (doi:10.2307/2411057)
27. Debat, V., Alibert, P., David, P., Paradis, E. & Auffray, J. C. 2000 Independence between developmental stability and canalization in the skull of the house mouse. Proc. R. Soc. Lond. B 267, 423-430. (doi:10.1098/rspb.2000.1017)
28. Mikula, O., Auffray, J. C. & Macholán, M. 2010 Asymmetric size and shape variation in the Central European transect across the house mouse hybrid zone. Biol. J. Linn. Soc. 101, 13-27. (doi:10.1111/j.1095-8312.2010.01490.x)
29. Haldane, J. B. S. 1922 Sex ratio and unisexual sterility in hybrid animals. J. Genet. 12, 101-109. (doi:10.1007/BF02983075)
30. Calvel, P., Rolland, A. D., Jegou, B. & Pineau, C. 2010 Testicular postgenomics: targeting the regulation of spermatogenesis. Phil. Trans. R. Soc. B 365, 1481-1500. (doi:10.1098/rstb.2009.0294)
31. Immler, S., Hamilton, M. B., Poslusny, N. J., Birkhead, T. R. & Epifanio, J. M. 2011 Post-mating reproductive barriers in two unidirectionally hybridizing sunfish (Centrarchidae: Lepomis). J. Evol. Biol. 24, 111-120. (doi:10.1111/j.1420-9101.2010.02142.x)
32. Dean, M. D., Ardlie, K. G. & Nachman, M. W. 2006 The frequency of multiple paternity suggests that sperm competition is common in house mice (Mus domesticus). Mol. Ecol. 15, 4141-4151. (doi:10.1111/j.1365-294X.2006.03068.x)
33. Howard, D. J., Palumbi, S. R., Birge, L. M. & Manier, M. K. 2009 Sperm and speciation. In Sperm biology: an evolutionary perspective (eds T. R. Birkhead, D. J. Hosken & S. Pitnick), pp. 367-403. Oxford, UK: Academic Press.
34. Pizzari, T. & Parker, G. A. 2009 Sperm competition and sperm phenotype. In Sperm biology: an evolutionary perspective (eds T. R. Birkhead, D. J. Hosken & S. Pitnick), pp. 207-245. Oxford, UK: Academic Press.
35. Kleven, O., Fossøy, F., Laskemoen, T., Robertson, R. J., Rudolfsen, G. & Lifjeld, J. T. 2009 Comparative evidence for the evolution of sperm swimming speed by sperm competition and female sperm storage duration in passerine birds. Evolution 63, 2466-2473. (doi:10.1111/j.1558-5646.2009.00725.x)
36. Vyskočilová, M., Pražanová, G. & Piálek, J. 2009 Polymorphism in hybrid male sterility in wild-derived Mus musculus musculus strains on proximal chromosome 17. Mamm. Genome 20, 83-91. (doi:10.1007/s00335-008-9164-3)
37. Munclinger, P., Boži{dotless}́ková, E., Šugerková, M., Piálek, J. & Macholán, M. 2002 Genetic variation in house mice (Mus, Muridae, Rodentia) from the Czech and Slovak Republics. Folia Zool. 51, 81-92.
38. Schielzeth, H. 2010 Simple means to improve the interpretability of regression coefficients. Methods Ecol. Evol. 1, 103-113. (doi:10.1111/j.2041-210X.2010.00012.x)
39. R Development Core Team 2005 R: a language and environment for statistical computing, reference index v. 2.13.1. Vienna, Austria: R Foundation for Statistical Computing. ISBN 3-900051-07-0, URL http://www.R-project.org.
40. Nelder, J. A. & Wedderburn, R. W. M. 1972 Generalized linear models. J. R. Stat. Soc. A 135, 370-384. (doi:10.2307/2344614)
41. Crawley, M. J. 2007 The R book. Chichester, UK: Wiley.
42. Raufaste, N., Orth, A., Belkhir, K., Senet, D., Smadja, C., Baird, S. J. E., Bonhomme, F., Dod, B. & Boursot, P. 2005 Inferences of selection and migration in the Danish house mouse hybrid zone. Biol. J. Linn. Soc. 84, 593-616. (doi:10.1111/j.1095-8312.2005.00457.x)
43. Virdee, S. R. & Hewitt, G. M. 1994 Clines for hybrid dysfunction in a grasshopper hybrid zone. Evolution 48, 392-407. (doi:10.2307/2410100)
44. Vyskočilová, M., Trachtulec, Z., Forejt, J. & Piálek, J. 2005 Does geography matter in hybrid sterility in house mice? Biol. J. Linn. Soc. 84, 663-674. (doi:10.1111/j.1095-8312.2005.00463.x)
45. Good, J. M., Handel, M. A. & Nachman, M. W. 2008 Asymmetry and polymorphism of hybrid male sterility during the early stages of speciation in housemice. Evolution 62, 50-65. (doi:10.1111/j.1558-5646.2007.00257.x)
46. Forejt, J. & Iványi, P. 1974 Genetic studies on male sterility of hybrids between laboratory and wild mice (Mus musculus L.). Genet. Res. 24, 189-206. (doi:10.1017/S0016672300015214)
47. Birkhead, T. R., Marti{dotless}́nez, J. G., Burke, T. & Froman, D. P. 1999 Sperm mobility determines the outcome of sperm competition in the domestic fowl. Proc. R. Soc. Lond. B 266, 1759-1764. (doi:10.1098/rspb.1999.0843)
48. Birkhead, T. R., Hosken, D. J. & Pitnick, S. 2009 Sperm biology: an evolutionary perspective. Oxford, UK: Academic Press.
49. Gomendio, M., Martin-Coello, J., Crespo, C., Magana, C. & Roldan, E. R. S. 2006 Sperm competition enhances functional capacity of mammalian spermatozoa. Proc. Natl Acad. Sci. USA 103, 15 113-15 117. (doi:10.1073/pnas.0605795103)
50. Gasparini, C., Simmons, L. W., Beveridge, M. & Evans, J. P. 2010 Sperm swimming velocity predicts competitive fertilization success in the green swordtail Xiphophorus helleri. PLoS ONE 5, e12146. (doi:10.1371/journal.pone.0012146)
51. Laskemoen, T., Kleven, O., Fossoy, F., Robertson, R. J., Rudolfsen, G. & Lifjeld, J. T. 2010 Sperm quantity and quality effects on fertilization success in a highly promiscuous passerine, the tree swallow Tachycineta bicolor. Behav. Ecol. Sociobiol. 64, 1473-1483. (doi:10.1007/s00265-010-0962-8)
52. Dean, M. D. & Nachman, M.W. 2009 Faster fertilization rate in conspecific versus heterospecific matings in house mice. Evolution 63, 20-28. (doi:10.1111/j.1558-5646.2008.00499.x)
53. Firman, R. C. & Simmons, L. W. 2008 The frequency of multiple paternity predicts variation in testes size among island populations of house mice. J. Evol. Biol. 21, 1524-1533. (doi:10.1111/j.1420-9101.2008.01612.x)
54. Piálek, J. et al. 2008 Development of unique house mouse resources suitable for evolutionary studies of speciation. J. Hered. 99, 34-44. (doi:10.1093/jhered/esm083)
55. Ďureje, L., Macholán, M., Baird, S. J. E. & Piálek, J. In press. The mouse hybrid zone in Central Europe: from morphology to molecules. Folia Zool.
56. Barton, N. H. & Bengtsson, B. O. 1986 The barrier to genetic exchange between hybridising populations. Heredity 56, 357-376. (doi:10.1038/hdy.1986.135)
57. Piálek, J. & Barton, N. H. 1997 The spread of an advantageous allele across a barrier: the effects of random drift and selection against heterozygotes. Genetics 145, 493-504.
58. Baird, S. J. E. & Macholán, M. 2012 What can the Mus musculus musculus/M. m. domesticus hybrid zone tell us about speciation? In Evolution of the house Mouse (eds M. Macholán, S. J. E. Baird, P. Munclinger & J. Piálek), pp. 334-372. Cambridge, UK: Cambridge University Press.
59. Rosenfeld, C. S., Grimm, K. M., Livingston, K. A., Brokman, A. M., Lamberson, W. E. & Roberts, R. M. 2003 Striking variation in the sex ratio of pups born to mice according to whether maternal diet is high in fat or carbohydrate. Proc. Natl Acad. Sci. USA 100, 4628-4632. (doi:10.1073/pnas.0330808100)
60. Fisher, R. A. 1930 The Genetical Theory of Natural Selection. Oxford, UK: Oxford University Press.
61. Trivers, R. L. & Willard, D. E. 1973 Natural selection of parental ability to vary sex ratio of offspring. Science 179, 90-792. (doi:10.1126/science.179.4068.90)
62. Janoušek, V. et al. 2012 Genome-wide architecture of reproductive isolation in a naturally occurring hybrid zone between Mus musculus musculus and M. m. domesticus. Mol. Ecol. 21, 3032-3047. (doi:10.1111/j.1365-294X.2012.05583.x)
63. Sackton, T. B., Montenegro, H., Hartl, D. L. & Lemos, B. 2011 Interspecific Y chromosome introgressions disrupt testis-specific gene expression and male reproductive phenotypes in Drosophila. Proc. Natl Acad. Sci. USA 108, 17 046-17 051. (doi:10.1073/pnas.1114690108)
64. Ellis, P. J. I., Bacon, J. & Affara, N. A. 2011 Association of Sly with sex-linked gene amplification during mouse evolution: a side effect of genomic conflict in spermatids? Hum. Mol. Genet. 20, 3010-3021. (doi:10.1093/hmg/ddr204)
65. Cocquet, J., Ellis, P. J. I., Yamauchi, Y., Mahadevaiah, S. K., Affara, N. A., Ward, M. A. & Burgoyne, P. S. 2009 The multicopy gene Sly represses the sex chromosomes in the male mouse germline after meiosis. PLoS Biol. 7, e1000244. (doi:10.1371/journal.pbio.1000244)