Atlantic salmon eggs favour sperm in competition that have similar major histocompatibility alleles

Proceedings of the Royal Society B: Biological Sciences

Volumn 276, Issue 1656, 2009, Pages 559-566

  Yeates, Sarah E ^a   Einum, Sigurd ^b   Fleming, Ian A ^c   Megens, Hendrik Jan ^d   Stet, René J M ^d   Hindar, Kjetil ^b   Holt, William V ^e   Van Look, Katrien J W ^e   Gage, Matthew J G ^a  

^a UNIVERSITY OF EAST ANGLIA   (United Kingdom)

^b NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^c MEMORIAL UNIVERSITY OF NEWFOUNDLAND   (Canada)

^d WAGENINGEN UNIVERSITY   (Netherlands)

^e INSTITUTE OF ZOOLOGY   (United Kingdom)

Author keywords

Atlantic salmon; Cryptic female choice; Fertilization; Major histocompatibility genes; Sperm competition

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1;

ALLELE; COPULATION; EVOLUTION; FERTILIZATION (REPRODUCTION); POLYANDRY; SALMONID; SEXUAL SELECTION; SPERM COMPETITION;

ALLELE; ARTICLE; ATLANTIC SALMON; EGG; EXPERIMENTAL DESIGN; FEMALE; FERTILIZATION IN VITRO; GAMETE; GENETIC VARIABILITY; HETEROZYGOSITY; IMMUNOGENETICS; MAJOR HISTOCOMPATIBILITY COMPLEX; MALE; MICROENVIRONMENT; NONHUMAN; PRIORITY JOURNAL; SPERM COMPETITION; SPERMATOZOON DENSITY;

SALMO SALAR;

EID: 58149124115     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2008.1257     Document Type: Article

References (63)

1. Arnaizvillena, A. & Festenstein, H. 1976 HLA genotyping by using spermatozoa: evidence for haploid gene-expression. Lancet 2, 707-709.
2. Bateson, P. 1978 Sexual imprinting and optimal outbreeding. Nature 273, 659-660.
3. Billard, R. & Cosson, M. P. 1992 Some problems related to the assessment of sperm motility in fresh-water fish. J. Exp. Zool. 261, 122-131.
4. Birkhead, T. R. 1998 Cryptic female choice: criteria for establishing female sperm choice. Evolution 52, 1212-1218.
5. Birkhead, T. & Moller, A. P. 1998 Sperm competition and sexual selection. San Diego, CA: Academic Press.
6. Bishop, J. D. D., Jones, C. S. & Noble, L. R. 1996 Female control of paternity in the internally fertilizing compound ascidian Diplosoma listerianum. 2. Investigation of male mating success using RAPD markers. Proc. R. Soc. B 263, 401-407.
7. Bonneaud, C., Chastel, O., Federici, P., Westerdahl, H. & Sorci, G. 2006 Complex MHC-based mate choice in a wild passerine. Proc. R. Soc. B 273, 1111-1116.
8. Cairney, M., Taggart, J. B. & Hoyheim, B. 2000 Characterization of microsatellite and minisatellite loci in Atlantic salmon (Salmo salar L.) and cross-species amplification in other salmonids. Mol. Ecol. 9, 2175-2178.
9. Consuegra, S. & García de Leániz, C. 2008 MHC-mediated mate choice increases parasite resistance in salmon. Proc. R. Soc. B 275, 1397-1403.
10. Consuegra, S., Megens, H. J., Schaschl, H., Leon, K., Stet, R. J. M. & Jordan, W. C. 2005 Rapid evolution of the MH class I locus results in different allelic compositions in recently diverged populations of Atlantic salmon. Mol. Biol. Evol. 22, 1095-1106.
11. Dionne, M., Miller, K. M., Dodson, J. J., Caron, F. & Bernatchez, L. 2007 Clinal variation in MHC diversity with temperature: evidence for the role of host-pathogen interaction on local adaptation in Atlantic salmon. Evolution 61, 2154-2164.
12. Doherty, P. C. & Zinkernagel, R. M. 1975 Enhanced immunological surveillance in mice heterozygous at H-2 gene complex. Nature 256, 50-52.
13. Eberhard, W. G. 1996 Female control: sexual selection by cryptic female choice. Princeton, NJ: Princeton University Press.
14. Edwards, S. V. & Hedrick, P. W. 1998 Evolution and ecology of MHC molecules: from genomics to sexual selection. Trends Ecol. Evol. 13, 305-311.
15. Fleming, I. A. 1996 Reproductive strategies of Atlantic salmon: ecology and evolution. Rev. Fish Biol. Fisheries 6, 379-416.
16. Fleming, I. A., Jonsson, B., Gross, M. R. & Lamberg, A. 1996 An experimental study of the reproductive behaviour and success of farmed and wild Atlantic salmon (Salmo salar). J. Appl. Ecol. 33, 893-905.
17. Forsberg, L. A., Dannewitz, J., Petersson, E. & Grahn, M. 2007 Influence of genetic dissimilarity in the reproductive success and mate choice of brown trout - females fishing for optimal MHC dissimilarity. J. Evol. Biol. 20, 1859-1869.
18. Freeman-Gallant, C. R., Meguerdichian, M., Wheelwright, N. T. & Sollecito, S. V. 2003 Social pairing and female mating fidelity predicted by restriction fragment length polymorphism similarity at the major histocompatibility complex in a songbird. Mol. Ecol. 12, 3077-3083.
19. Gage, M. J. G., Stockley, P. & Parker, G. A. 1998 Sperm morphometry in the Atlantic salmon. J. Fish Biol. 53, 835-840.
20. Gage, M. J. G., Macfarlane, C. P., Yeates, S., Ward, R. G., Searle, J. B. & Parker, G. A. 2004 Spermatozoal traits and sperm competition in Atlantic salmon: relative sperm velocity is the primary determinant of fertilization success. Curr. Biol. 14, 44-47.
21. Galindo, B. E., Vacquier, V. D. & Swanson, W. J. 2003 Positive selection in the egg receptor for abalone sperm lysin. Proc. Natl Acad. Sci. USA 100, 4639-4643.
22. Garant, D., Dodson, J. J. & Bernatchez, L. 2000 Ecological determinants and temporal stability of the within-river population structure in Atlantic salmon (Salmo salar). Mol. Ecol. 9, 615-628.
23. Garcia-Vazquez, E., Moran, P., Martinez, J. L., Perez, J., de Gaudemar, B. & Beall, E. 2001 Alternative mating strategies in Atlantic salmon and brown trout. J. Hered. 92, 146-149.
24. Gilkey, J. C. 1981 Mechanisms of fertilization in fishes. Am. Zool. 21, 359-375.
25. Grimholt, U., Drablos, F., Jorgensen, S. M., Hoyheim, B. & Stet, R. J. M. 2002 The major histocompatibility class I locus in Atlantic salmon (Salmo salar): polymorphism, linkage analysis and protein modelling. Immunogenetics 54, 570-581.
26. Haas, G. G. & Nahhas, F. N. 1986 Quantification of antisperm antibodies by an indirect inhibition assay. J. Androl. 7, P15-P15.
27. Hoysak, D. J. & Liley, N. R. 2001 Fertilization dynamics in sockeye salmon and a comparison of sperm from alternative male phenotypes. J. Fish Biol. 58, 1286-1300.
28. Jeffery, K. J. M. & Bangham, C. R. M. 2000 Do infectious diseases drive MHC diversity? Microbes Infect. 2, 1335-1341.
29. Kime, D. E., Van Look, K. J. W., McAllister, B. G., Huyskens, G., Rurangwa, E. & Ollevier, F. 2001 Computer-assisted sperm analysis (CASA) as a tool for monitoring sperm quality in fish. Comp. Biochem. Physiol. C-Toxicol. Pharmacol. 130, 425-433.
30. Klein, J. 1986 The natural history of the major histocompatibility complex. New York, NY: Wiley.
31. Kobayashi, W. & Yamamoto, T. S. 1981 Fine-structure of the micropylar apparatus of the chum salmon egg, with a discussion of the mechanism for blocking polyspermy. J. Exp. Zool. 217, 265-275.
32. Landry, C. & Bernatchez, L. 2001 Comparative analysis of population structure across environments and geographical scales at major histocompatibility complex and microsatellite loci in Atlantic salmon (Salmo salar). Mol. Ecol. 10, 2525-2539.
33. Landry, C., Garant, D., Duchesne, P. & Bernatchez, L. 2001 'Good genes as heterozygosity': the major histocompatibility complex and mate choice in Atlantic salmon (Salmo salar). Proc. R. Soc. B 268, 1279-1285.
34. Lohm, J., Grahn, M., Langefors, A., Andersen, O., Storset, A. & von Schantz, T. 2002 Experimental evidence for major histocompatibility complex- allele-specific resistance to a bacterial infection. Proc. R. Soc. B 269, 2029-2033.
35. Lynch, M. 1991 The genetic interpretation of inbreeding depression and outbreeding depression. Evolution 45, 622-629.
36. Metz, E. C. & Palumbi, S. R. 1996 Positive selection and sequence rearrangements generate extensive polymorphism in the gamete recognition protein bindin. Mol. Biol. Evol. 13, 397-406.
37. Neff, B. D., Garner, S. R., Heath, J. W. & Heath, D. D. 2008 The MHC and non-random mating in a captive population of Chinook salmon. Heredity 101, 175-185.
38. Ober, C., Weitkamp, L. R., Cox, N., Dytch, H., Kostyu, D. & Elias, S. 1997 HLA and mate choice in humans. Am. J. Hum. Genet. 61, 497-504.
39. Palumbi, S. R. 1999 All males are not created equal: fertility differences depend on gamete recognition polymorphisms in sea urchins. Proc. Natl Acad. Sci. USA 96, 12 632-12 637.
40. Parker, G. A. 1970 Sperm competition and its evolutionary consequences in insects. Biol. Rev. Camb. Philos. Soc. 45, 525-567.
41. Penn, D. & Potts, W. 1998 MHC-disassortative mating preferences reversed by cross- fostering. Proc. R. Soc. B 265, 1299-1306.
42. Piertney, S. B. & Oliver, M. K. 2006 The evolutionary ecology of the major histocompatibility complex. Heredity 96, 7-21.
43. Pilastro, A., Simonato, M., Bisazza, A. & Evans, J. P. 2004 Cryptic female preference for colorful males in guppies. Evolution 58, 665-669.
44. Pitcher, T. E. & Neff, B. D. 2006 MHC class IIB alleles contribute to both additive and non-additive genetic effects on survival in Chinook salmon. Mol. Ecol. 15, 2357-2365.
45. Pizzari, T. & Birkhead, T. R. 2000 Female feral fowl eject sperm of subdominant males. Nature 405, 787-789.
46. Potts, W. K. & Wakeland, E. K. 1990 Evolution of diversity at the major histocompatibility complex. Trends Ecol. Evol. 5, 181-187.
47. Potts, W. K., Manning, C. J. & Wakeland, E. K. 1991 Mating patterns in seminatural populations of mice influenced by MHC genotype. Nature 352, 619-621.
48. Reusch, T. B. H., Haberli, M. A., Aeschlimann, P. B. & Milinski, M. 2001 Female sticklebacks count alleles in a strategy of sexual selection explaining MHC polymorphism. Nature 414, 300-302.
49. Richardson, D. S., Komdeur, J., Burke, T. & von Schantz, T. 2005 MHC-based patterns of social and extra-pair mate choice in the Seychelles warbler. Proc. R. Soc. B 272, 759-767.
50. Robinson, J., Malik, A., Parham, P., Bodmer, J. G. & Marsh, S. G. E. 2000 IMGT/HLA database: a sequence database for the human major histocompatibility complex. Tissue Antigens 55, 280-287.
51. Scofield, V. L., Schlumpberger, J. M., West, L. A. & Weissman, I. L. 1982 Protochordate allorecognition is controlled by a MHC-like gene system. Nature 295, 499-502.
52. Skarstein, F., Folstad, I., Liljedal, S. & Grahn, M. 2005 MHC and fertilization success in the Arctic charr (Salvelinus alpinus). Behav. Ecol. Sociobiol. 57, 374-380.
53. Swanson, W. J. & Vacquier, V. D. 1997 The abalone egg vitelline envelope receptor for sperm lysin is a giant multivalent molecule. Proc. Natl Acad. Sci. USA 94, 6724-6729.
54. Swanson, W. J., Aquadro, C. F. & Vacquier, V. D. 2001 Polymorphism in abalone fertilization proteins is consistent with the neutral evolution of the egg's receptor for lysin (VERL) and positive Darwinian selection of sperm lysin. Mol. Biol. Evol. 18, 376-383.
55. Taylor, E. B. 1991 A review of local adaptation in Salmonidae, with particular reference to Pacific and Atlantic salmon. Aquaculture 98, 185-207.
56. Vacquier, V. D., Swanson, W. J. & Hellberg, M. E. 1995 What havewe learned about sea-urchin spermbindin. Dev. Growth Differ. 37, 1-10.
57. Wagner, E., Arndt, R. & Hilton, B. 2002 Physiological stress responses, egg survival and sperm motility for rainbow trout broodstock anesthetized with clove oil, tricaine methanesulfonate or carbon dioxide. Aquaculture 211, 353-366.
58. Wedekind, C. & Furi, S. 1997 Body odour preferences in men and women: do they aim for specific MHC combinations or simply heterozygosity? Proc. R. Soc. B 264, 1471-1479.
59. Wedekind, C., Seebeck, T., Bettens, F. & Paepke, A. J. 1995 MHC-dependent mate preferences in humans. Proc. R. Soc. B 260, 245-249.
60. Wedekind, C., Chapuisat, M., Macas, E. & Rulicke, T. 1996 Non-random fertilization in mice correlates with the MHC and something else. Heredity 77, 400-409.
61. Wedekind, C., Walker, M., Portmann, J., Cenni, B., Muller, R. & Binz, T. 2004 MHC-linked susceptibility to a bacterial infection, but no MHC- linked cryptic female choice in whitefish. J. Evol. Biol. 17, 11-18.
62. Yamazaki, K., Boyse, E. A., Mike, V., Thaler, H. T., Mathieson, B. J., Abbott, J., Boyse, J., Zayas, Z. A. & Thomas, L. 1976 Control of mating preferences in mice by genes in major histocompatibility complex. J. Exp. Med. 144, 1324-1335.
63. Yeates, S., Searle, J., Ward, R. G. & Gage, M. J. G. 2007 A two-second delay confers first-male fertilization precedence within in vitro sperm competition experiments in Atlantic salmon. J. Fish Biol. 70, 318-322.