Sexual conflict inhibits female mate choice for major histocompatibility complex dissimilarity in Chinook salmon http://rspb.royalsocietypublishing.org/ subscriptions

Proceedings of the Royal Society B: Biological Sciences

Volumn 277, Issue 1683, 2010, Pages 885-894

  Garner, Shawn R ^a   Bortoluzzi, Romina N ^b   Heath, Daniel D ^b   Neff, Bryan D ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b UNIVERSITY OF WINDSOR   (Canada)

Author keywords

Coercive mating; Major histocompatibility complex; Mate choice; Salmonids; Sexual selection

Indexed keywords

AGGRESSION; LIFE HISTORY TRAIT; MATE CHOICE; PEPTIDE; REPRODUCTIVE SUCCESS; SALMONID; SEX RATIO; SEXUAL CONFLICT; SEXUAL SELECTION; SPAWNING;

ONCORHYNCHUS TSHAWYTSCHA; SALMONIDAE;

EID: 77950192919     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2009.1639     Document Type: Article

References (63)

1. Arkush, K. D., Giese, A. R., Mendonca, H. L., McBride, A. M., Marty, G. D. & Hedrick, P. W. 2002 Resistance to three pathogens in the endangered winter-run Chinook salmon (Oncorhynchus tshawytscha): effects of inbreeding and major histocompatibility complex genotypes. Can. J. Fish. Aquat. Sci. 59, 966-975. (doi:10.1139/ f02-066)
2. Arnqvist, G. & Rowe, L. 2005 Sexual conflict. Princeton, NJ: Princeton University Press.
3. Bateman, A. J. 1948 Intra-sexual selection in Drosophila. Heredity 2, 349-368. (doi:10.1038/hdy.1948.21)
4. Beacham, T. D. 1984 Age and morphology of chum salmon in Southern British Columbia. Trans. Am. Fish. Soc. 113, 727-736. (doi:10.1577/1548-8659(1984) 113<727: AAMOCS>2.0.CO;2)
5. Berejikian, B. A., Tezak, E. P. & LaRae, A. L. 2000 Female mate choice and spawning behaviour of Chinook salmon under experimental conditions. J. Fish Biol. 57, 647-661. (doi:0.1111/j.1095-8649.2000.tb00266.x)
6. Bernatchez, L. & Landry, C. 2003 MHC studies in nonmodel vertebrates: what have we learned about natural selection in 15 years? J. Evol. Biol. 16, 363-377. (doi:10.1046/j.1420-9101.2003.00531.x)
7. Blanckenhorn,W. U., Hosken, D. J., Martin, O. Y., Reim, C., Teuschl, Y. & Ward, P. I. 2002 The costs of copulating in the dung fly Sepsis cynipsea. Behav. Ecol. 13, 353-358. (doi:10.1093/beheco/13.3.353)
8. Brown, J. H., Jardetzky, T., Saper, M. A., Samraoui, B., Bjorkman, P. J. & Wiley, D. C. 1988 A hypothetical model of the foreign antigen-binding site of class II histocompatibility molecules. Nature 332, 845-850. (doi:10. 1038/332845a0)
9. Casalini, M., Agbali, M., Reichard, M., Konečná, M., Bryjová, A. & Smith, C. 2009 Male dominance, female mate choice, and intersexual conflict in the rose bitterling (Rhodeus ocellatus). Evolution 63, 366-376. (doi:10.1111/ j.1558-5646.2008.00555.x)
10. Clutton-Brock, T. H. & Parker, G. A. 1992 Potential reproductive rates and the operation of sexual selection. Q. Rev. Biol. 67, 437-456. (doi:10.1086/417793)
11. Clutton-Brock, T. H. & Parker, G. A. 1995 Sexual coercion in animal societies. Anim. Behav. 49, 1345-1365. (doi:10. 1006/anbe.1995.0166)
12. Clutton-Brock, T. H., Green, D., Hiraiwa-Hasegawa, M. & Albon, S. D. 1988 Passing the buck: resource defence, lek breeding and mate choice in fallow deer. Behav. Ecol. Sociobiol. 23, 281-296. (doi:10.1007/BF00300575)
13. Docker, M. F. & Heath, D. D. 2002 PCR-based markers detect genetic variation at growth and immune functionrelated loci in Chinook salmon (Oncorhynchus tshawytscha). Mol. Ecol. Notes 2, 606-609. (doi:10.1046/ j.1471-8286.2002.00315.x)
14. Doherty, P. C. & Zinkernagel, R. M. 1975 Enhanced immunological surveillance in mice heterozygous at the H-2 gene complex. Nature 256, 50-52. (doi:10.1038/ 256050a0)
15. Eizaguirre, C., Yeates, S. E., Lenz, T. L., Kalbe, M. & Milinski, M. 2009 MHC-based mate choice combines good genes and maintenance of MHC polymorphism. Mol. Ecol. 18, 3316-3329. (doi:10.1111/j.1365-294X. 2009.04243.x)
16. Emlen, S. T. & Oring, L. W. 1977 Ecology, sexual selection, and the evolution of mating systems. Science 197, 215-223. (doi:10.1126/science.327542)
17. Fleming, I. A. 1998 Pattern and variability in the breeding system of Atlantic salmon (Salmo salar), with comparisons to other salmonids. Can. J. Fish. Aquat. Sci. 55(Suppl. 1), 59-76. (doi:10.1139/cjfas-55-S1-59)
18. Fleming, I. A. & Gross, M. R. 1994 Breeding competition in a Pacific salmon (Coho: Oncorhynchus kisutch): measures of natural and sexual selection. Evolution 48, 637-657. (doi:10.2307/2410475)
19. Fleming, I. A., Lamberg, A. & Jonsson, B. 1997 Effects of early experience on the reproductive performance of Atlantic salmon. Behav. Ecol. 8, 470-480. (doi:10.1093/ beheco/8.5.470)
20. Foote, C. J. 1989 Female mate preference in Pacific salmon. Anim. Behav. 38, 721-723. (doi:10.1016/S0003-3472(89) 80022-3)
21. 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. (doi:10.1111/j.1420-9101.2007.01380.x)
22. 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. (doi:10.1046/j.1365-294X.2003.01968.x)
23. Heath, D. D., Rankin, L., Bryden, C. A., Heath, J. W. & Shrimpton, J. M. 2002 Heritability and Y-chromosome influence in the jack male life history of Chinook salmon (Oncorhynchus tshawytscha). Heredity 89, 311-317. (doi:10.1038/sj.hdy.6800141)
24. Janeway, C. A., Travers, P., Walport, M. & Capra, J. D. 1999 Immunobiology: the immune system in health and disease. London, UK: Current Biology Publications.
25. Jirotkul, M. 1999 Operational sex ratio influences female preference and male-male competition in guppies. Anim. Behav. 58, 287-294. (doi:10.1006/anbe. 1999.1149)
26. Kalbe, M., Eizaguirre, C., Dankert, I., Reusch, T. B. H., Sommerfeld, R. D., Wegner, K. M. & Milinski, M. 2009 Lifetime reproductive success is maximized with optimal major histocompatibility complex diversity. Proc. R. Soc. B 276, 925-934. (doi:10.1098/rspb.2008. 1466)
27. Kalinowski, S. T., Taper, M. L. & Marshall, T. C. 2007 Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol. Ecol. 16, 1099-1106. (doi:10.1111/ j.1365-294X.2007.03089.x)
28. Kim, T. J., Parker, K. M. & Hedrick, P. W. 1999 Major histocompatibility complex differentiation in Sacramento River Chinook salmon. Genetics 151, 1115-1122.
29. Kurtz, J., Kalbe, M., Aeschlimann, P. B., Häberli, M. A., Wegner, K. M., Reusch, T. B. H. & Milinski, M. 2004 Major histocompatibility complex diversity influences parasite resistance and innate immunity in sticklebacks. Proc. R. Soc. Lond. B 271, 197-204. (doi:10.1098/rspb. 2003.2567)
30. Kvarnemo, C. & Ahnesjo, I. 1996 The dynamics of operational sex ratios and competition for mates. Trends Ecol. Evol. 11, 404-408. (doi:10.1016/0169-5347(96) 10056-2)
31. 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. Lond. B 268, 1279-1285. (doi:10.1098/rspb.2001.1659)
32. Le Boeuf, B. J. & Mesnick, S. 1991 Sexual behavior of male northern elephant seals: I. Lethal injuries to adult females. Behaviour 116, 143-162. (doi:10.1163/ 156853990X00400)
33. Magurran, A. E. & Nowak, M. A. 1991 Another battle of the sexes: the consequences of sexual asymmetry in mating costs and predation risk in the guppy Poecilia reticulata. Proc. R. Soc. Lond. B 246, 31-38. (doi:10.1098/rspb. 1991.0121)
34. Magurran, A. E. & Seghers, B. H. 1994a A cost of sexual harassment in the guppy Poecilia reticulata. Proc. R. Soc. Lond. B 258, 89-92. (doi:10.1098/rspb.1994.0147)
35. Magurran, A. E. & Seghers, B. H. 1994b Sexual conflict as a consequence of ecology: evidence from guppy, Poecilia reticulata, populations in Trinidad. Proc. R. Soc. Lond. B 255, 31-36. (doi:10.1098/rspb.1994.0005)
36. Manly, B. F. J. 1997 In Randomization, bootstrapping and Monte Carlo methods in biology. London, UK: Chapman & Hall.
37. Marshall, T. C., Slate, J., Kruuk, L. E. B. & Pemberton, J. M. 1998 Statistical confidence for likelihood-based paternity inference in natural populations. Mol. Ecol. 7, 639-655. (doi:10.1046/j.1365-294x.1998.00374.x)
38. Milinski, M., Griffiths, S., Wegner, K. M., Reusch, T. B. H., Haas-Assenbaum, A. & Boehm, T. 2005 Mate choice decisions of stickleback females predictably modified by MHC peptide ligands. Proc. Natl Acad. Sci. USA 102, 4414-4418. (doi:10.1073/pnas.0408264102)
39. Miller, K. M. & Withler, R. E. 1996 Sequence analysis of a polymorphic MHC class II gene in Pacific salmon. Immunogenetics 43, 337-351. (doi:10.1007/BF02199802)
40. Neff, B. D. & Pitcher, T. E. 2005 Genetic quality and sexual selection: an integrated framework for good genes and compatible genes. Mol. Ecol. 14, 19-38. (doi:10.1111/ j.1365-294X.2004.02395.x)
41. 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. (doi:10.1038/hdy.2008.43)
42. Nowak, M. A., Tarczy-Hornoch, K. & Austyn, J. M. 1992 The optimal number of major histocompatibility complex molecules in an individual. Proc. Natl Acad. Sci. USA 89, 10896-10899. (doi:10.1073/pnas.89.22.10896)
43. 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. (doi:10.1086/515511)
44. Olsén, K. H., Grahn, M., Lohm, J. & Langefors, Å . 1998 MHC and kin discrimination in juvenile Arctic charr, Salvelinus alpinus (L.). Anim. Behav. 56, 319-327. (doi:10.1006/anbe.1998.0837)
45. Penn, D. J. 2002 The scent of genetic compatibility: sexual selection and the major histocompatibility complex. Ethology 108, 1-21. (doi:10.1046/j.1439- 0310.2002. 00768.x)
46. Pitcher, T. E. & Neff, B. D. 2006 MHC class IIB alleles contribute to both additive and nonadditive genetic effects on survival in Chinook salmon. Mol. Ecol. 15, 2357-2365. (doi:10.1111/j.1365-294X.2006.02942.x)
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. (doi:10.1038/ 352619a0)
48. Quinn, T. P. 2005 The behaviour and ecology of Pacific salmon and trout. Seattle, WA: University of Washington Press.
49. Quinn, T. P. & Foote, C. J. 1994 The effects of body size and sexual dimorphism on the reproductive behaviour of sockeye salmon, Oncorhynchus nerka. Anim. Behav. 48, 751-761. (doi:10.1006/anbe.1994.1300)
50. 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. (doi: 10.1038/35104547)
51. Roberts, S. C. & Gosling, L. M. 2003 Genetic similarity and quality interact in mate choice decisions by female mice. Nat. Genet. 35, 103-106. (doi:10.1038/ng1231)
52. Rowe, L. 1994 The costs of mating and mate choice in water striders. Anim. Behav. 48, 1049-1056. (doi:10.1006/ anbe.1994.1338)
53. Shum, B. P., Guethlein, L., Flodin, L. R., Adkison, M. A., Hedrick, R. P., Nehring, R. B., Stet, R. J. M., Secombes, C. & Parham, P. 2001 Modes of salmonid MHC class I and II evolution differ from the primate paradigm. J. Immunol. 166, 3297-3308.
54. Sih, A. & Krupa, J. J. 1995 Interacting effects of prédation risk and male and female density on male-female conflicts and mating dynamics of stream water striders. Behav. Ecol. 6, 316-325. (doi:10.1093/beheco/6.3.316)
55. Smith, C. C. & Sargent, R. C. 2006 Female fitness declines with increasing female density but not male harassment in the western mosquitofish Gambusia affinis. Anim. Behav. 71, 401-407. (doi:10.1016/j.anbehav.2005.06.003)
56. Smuts, B. B. & Smuts, R. W. 1993 Male aggression and sexual coercion of females in nonhuman primates and other mammals: evidence and theoretical implications. Adv. Study Behav. 22, 1-63. (doi:10.1016/S0065-3454(08)60404-0)
57. Trivers, R. L. 1972 Parental investment and sexual selection. In Sexual selection and the descent of man (ed. B. Campbell), pp. 136-179. Chicago, IL: Aldine.
58. Turner, S. M., Faisal, M. & DeWoody, J. A. 2007 Zygosity at the major histocompatibility class IIB locus predicts susceptibility to Renibacterium salmoninarum in Atlantic salmon (Salmo salar L.). Anim. Genet. 38, 517-519. (doi:10.1111/j.1365-2052.2007.01631.x)
59. Wakeland, E. K., Boehme, S., She, J. X., Lu, C. C., McIndoe, R. A., Cheng, I., Ye, Y. & Potts, W. K. 1990 Ancestral polymorphisms of MHC class II genes: divergent allele advantage. Immunol. Res. 9, 115-122.
60. Watters, J. V. 2005 Can the alternative male tactics 'fighter' and 'sneaker' be considered 'coercer' and 'cooperator' in coho salmon? Anim. Behav. 70, 1055-1062. (doi:10. 1016/j.anbehav.2005.01.025)
61. Wedekind, C. & Füri, S. 1997 Body odour preferences in men and women: do they aim for specific MHC combinations or simply heterozygosity? Proc. R. Soc. Lond. B 264, 1471-1479. (doi: 10.1098/rspb. 1997.0204)
62. Wegner, K. M., Kalbe, M., Kurtz, J., Reusch, T. B. H. & Milinski, M. 2003 Parasite selection for immunogenetic optimality. Science 301, 1343-1343 (doi:10.1126/ science. 10882)
63. Woelfing, B., Traulsen, A., Milinski, M. & Boehm, T. 2009 Does intra-individual major histocompatibility complex diversity keep a golden mean? Phil. Trans. R. Soc. B 364, 117-128. (doi:10.1098/rstb.2008.0174)