Individual MHC class I and MHC class IIB diversities are associated with male and female reproductive traits in the three-spined stickleback

Journal of Evolutionary Biology

Volumn 20, Issue 5, 2007, Pages 2005-2015

  Jager I ^a   Eizaguirre, C ^a   Griffiths, S W ^a   Kalbe, M ^a   Krobbach, C K ^a   Reusch, T B H ^a   Schaschl, H ^a   Milinski, M ^a  

^a MAX PLANCK INSTITUTE FOR EVOLUTIONARY BIOLOGY   (Germany)

Author keywords

Female reproduction; Gasterosteus aculeatus; Male breeding colouration; MHC class I; MHC class IIB; Negative frequency dependent selection; Nest quality

Indexed keywords

ALLELE; FISH; MAJOR HISTOCOMPATIBILITY COMPLEX; NEST; REPRODUCTIVE CYCLE; REPRODUCTIVE STATUS;

ALLELE; ANIMAL; ARTICLE; BREEDING; CLUTCH SIZE; COLOR; FEMALE; GENE; GENETIC VARIABILITY; GENETICS; HISTOLOGY; MALE; NESTING; PHYSIOLOGY; REPRODUCTION; SEXUAL SELECTION; SMEGMAMORPHA;

ALLELES; ANIMALS; BREEDING; CLUTCH SIZE; COLOR; FEMALE; GENES, MHC CLASS I; GENES, MHC CLASS II; MALE; MATING PREFERENCE, ANIMAL; NESTING BEHAVIOR; REPRODUCTION; SMEGMAMORPHA; VARIATION (GENETICS);

GASTEROSTEUS ACULEATUS; VERTEBRATA;

EID: 34547891023     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/j.1420-9101.2007.01366.x     Document Type: Article

References (66)

1. Aeschlimann, P.B., Häberli, M.A., Reusch, T.B.H., Boehm, T. Milinski, M. 2003. Female sticklebacks Gasterosteus aculeatus use self-reference to optimize MHC allele number during mate selection. Behav. Ecol. Sociobiol. 54 : 119 126.
2. Ananth, C.V. Kleinbaum, D. 1997. Regression models for ordinal responses: a review of methods and applications. Int. J. Epidemiol. 26 : 1323 1333.
3. Bakker, T.C.M. Milinski, M. 1991. Sequential female choice and the previous male effect in sticklebacks. Behav. Ecol. Sociobiol. 29 : 205 210.
4. Barber, I., Arnott, S.A., Braithwaite, V.A., Andrew, J., Mullen, W. Huntingford, F.A. 2000. Carotenoid-based sexual coloration and body condition in nesting male sticklebacks. J. Fish Biol. 57 : 777 790.
5. Barber, I., Arnott, S.A., Braithwaite, V.A., Andrew, J. Huntingford, F.A. 2001a. Indirect fitness consequences of mate choice in sticklebacks: offspring of brighter males grow slowly but resist parasitic infections. Proc. R. Soc. Lond. B 268 : 71 76.
6. Barber, I., Nairn, D. Huntingford, F.A. 2001b. Nests as ornaments: revealing construction by male sticklebacks. Behav. Ecol. 12 : 390 396.
7. Binz, T., Reusch, T.B.H., Wedekind, C. Milinski, M. 2001. SSCP analysis of MHC class IIB genes in the three-spined stickleback. J. Fish Biol. 58 : 887 890.
8. Bonneaud, C., Mazuc, J., Chastel, O., Westerdahl, H. Sorci, G. 2004. Terminal investment induced by immune challenge and fitness traits associated with major histocompatibility complex in the house sparrow. Evolution 58 : 2823 2830.
9. Bonneaud, C., Richard, M., Faivre, B., Westerdahl, H. Sorci, G. 2005. An MHC class I allele associated to the expression of T-dependent immune response in the house sparrow. Immunogenetics 57 : 782 789.
10. Bonneaud, C., Chastel, O., Federici, P., Westerdahl, H. Sorci, G. 2006. Complex MHC-based mate choice in a wild passerine. Proc. R. Soc. Lond. B 273 : 1111 1116.
11. Borghans, J.A.M., Noest, A.J. De Boer, R.J. 2003. Thymic selection does not limit the individual MHC diversity. Eur. J. Immunol. 33 : 3353 3358.
12. Bray, J.R. Curtis, D.R. 1957. An ordination of the upland forest communities of Southern Wisconsin. Ecol. Monogr. 27 : 325 349.
13. Brush, A.H. Reisman, H.M. 1965. The carotenoid pigments in the three-spined stickleback, Gasterosteus aculeatus. Comp. Biochem. Physiol. 14 : 121 125.
14. Candolin, U. Voigt, H.R. 2001. No effect of a parasite on reproduction in stickleback males: a laboratory artefact Parasitology 122 : 457 464.
15. Clarke, K.R. Gorley, R.N. 2006. PRIMER v6: User Manual/Tutorial. PRIMER-E, Plymouth, UK.
16. Clarke, K.R., Sommerfeld, P.J. Chapman, M.G. 2006. On resemblance measures for ecological studies, including taxonomic dissimilarities and a zero-adjusted Bray-Curtis coefficient for denuded assemblages. J. Exp. Mar. Biol. Ecol. 330 : 50 80.
17. De Boer, R.J. Perelson, A.S. 1993. How diverse should the immune system be Proc. R. Soc. Lond. B 252 : 171 175.
18. Fletcher, D.A. Wootton, R.J. 1995. A hierarchical response to differences in ration size in the reproductive performance of female three-spined sticklebacks. J. Fish Biol. 46 : 657 668.
19. Fox, J. Andersen, R. 2004. Effect Displays for Multinomial and Proportional-odds Logit Models. Revised version of paper read at the ASA Methodology conference. McMaster University, Hamilton, Canada.
20. Frischknecht, M. 1993. The breeding colouration of male three-spined sticklebacks (Gasterosteus aculeatus) as an indicator of energy investment in vigour. Evol. Ecol. 7 : 439 450.
21. Goldrath, A.W. Bevan, M.J. 1999. Selecting and maintaining a diverse T-cell repertoire. Nature 402 : 255 262.
22. Grimholt, U., Larsen, S., Nordmo, R., Midtlyng, P., Kjoeglum, S., Storset, A., Saebo, S. Stet, R.J.M. 2003. MHC polymorphism and disease resistance in Atlantic salmon (Salmo salar); facing pathogens with single expressed major histocompatibility class I and class II loci. Immunogenetics 55 : 210 219.
23. Hamilton, W.D. Zuk, M. 1982. Heritable true fitness and bright birds: a role for parasites Science 218 : 384 387.
24. Harf, R. Sommer, S. 2005. Association between major histocompatibility complex class II DRB alleles and parasite load in the hairy-footed gerbil, Gerbillurus paeba, in the southern Kalahari. Mol. Ecol. 14 : 85 91.
25. Hedrick, P.W. Kim, T.J. 1999. Genetics of complex polymorphisms: parasites and maintenance of MHC variation. In: Genetics, Evolution and Society (R. Singh & Co. Krimbas, eds), pp. 204-234. Harvard University Press, Cambridge, MA.
26. Janeway, C.A., Travers, P., Walport, M. Capra, J.D. 2001. Immunobiology: The Immune System in Health and Disease. Current Biology Publications, London.
27. Kurtz, J., Kalbe, M., Aeschlimann, P.B., Haberli, 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.
28. Kurtz, J., Wegner, K.M., Kalbe, M., Reusch, T.B.H., Schaschl, H., Hasselquist, D. Milinski, M. 2006. MHC genes and oxidative stress in sticklebacks - an immuno-ecological approach. Proc. R. Soc. Lond. B 273 : 1407 1414.
29. Langefors, Å., Lohm, J., Grahn, M., Andersen, Ø. von Schantz, T. 2001. Association between major histocompatibility complex class IIB alleles and resistance to Aeromonas salmonicida in Atlantic salmon. Proc. R. Soc. Lond. B 268 : 479 485.
30. Lawlor, D.A., Zemmour, J., Ennis, P.D. Parham, P. 1990. Evolution of class-I MHC genes and proteins: from natural selection to thymic selection. Annu. Rev. Immunol. 8 : 23 63.
31. Madsen, T. Ujvari, B. 2006. MHC class I variation associates with parasite resistance and longevity in tropical pythons. J. Evol. Biol. 19 : 1973 1978.
32. McLennan, D.A. McPhail, J.D. 1990. Experimental investigations of the evolutionary significance of sexually dimorphic nuptial coloration in Gasterosteus aculeatus (L): the relationship between male color and female behavior. Can. J. Zool. 68 : 482 492.
33. Milinski, M. 2003. The function of mate choice in sticklebacks: optimizing MHC genetics. J. Fish Biol. 63 (Suppl. S1 S16.
34. Milinski, M. 2006. The major histocompatibility complex (MHC), sexual selection and mate choice. Annu. Rev. Evol. Syst. 37 : 159 186.
35. Milinski, M. Bakker, T.C.M. 1990. Female sticklebacks use male coloration in mate choice and hence avoid parasitized males. Nature 344 : 330 333.
36. Milinski, M. Bakker, T.C.M. 1991. Sexual selection: female sticklebacks recognize a male's parasitization by its breeding coloration. Verh. Dtsch. Zool. Ges. 991 : 320.
37. Milinski, M. Bakker, T.C.M. 1992. Costs influence sequential mate choice in sticklebacks, Gasterosteus aculeatus. Proc. R. Soc. Lond. B 250 : 229 233.
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. U.S.A. 102 : 4414 4418.
39. 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. U.S.A. 89 : 10896 10899.
40. Olsson, M., Madsen, T., Nordby, J., Wapstra, E., Ujvari, B. Wittsell, H. 2003. Major histocompatibility complex and mate choice in sand lizards. Proc. R. Soc. Lond. B 270 (Suppl. S254 S256.
41. Paterson, S., Wilson, K. Pemberton, J.M. 1998. Major histocompatibility complex variation associated with juvenile survival and parasite resistance in a large unmanaged ungulate population (Ovies aries L.). Proc. Natl Acad. Sci. U.S.A. 95 : 3714 3719.
42. Penn, D.J. 2002. The scent of genetic compatibility: sexual selection and the major histocompatibility complex. Ethology 108 : 1 21.
43. Penn, D.J. Potts, W.K. 1999. The evolution of mating preferences and major histocompatibility complex genes. Am. Nat. 153 : 145 164.
44. 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.
45. Rauch, G., Kalbe, M. Reusch, T.B.H. 2006. Relative importance of MHC and genetic background for parasite load in a field experiment. Evol. Ecol. Res. 8 : 373 386.
46. Reusch, T.B.H. Langefors, Å. 2005. Inter- and intralocus recombination drive MHC class IIB gene diversification in a teleost, the three-spined stickleback Gasterosteus aculeatus. J. Mol. Evol. 61 : 531 541.
47. Reusch, T.B.H., Häberli, 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.
48. Reusch, T.B.H., Schaschl, H. Wegner, K.M. 2004. Recent duplication and inter-locus gene conversion in major histocompatibility class II genes in a teleost, the three-spined stickleback. Immunogenetics 56 : 427 437.
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. Lond. B 272 : 759 767.
50. Rowland, W.J. 1995. Do female sticklebacks care about male courtship vigour? Manipulation of display tempo using video playback. Behaviour 132 : 951 961.
51. Sato, A., Figueroa, F., O'hUigin, C., Steck, N. Klein, J. 1998. Cloning of major histocompatibility complex (MHC) genes from threespine stickleback, Gasterosteus aculeatus. Mol. Mar. Biol. Biotechnol. 7 : 221 231.
52. Sato, A., Figueroa, F., Murray, B.W., Málaga-Trillo, E., Zaleska-Rutczynska, Z., Sültmann, H., Toyosawa, S., Wedekind, C., Steck, N. Klein, J. 2000. Nonlinkage of major histocompatibility complex class I and class II loci in bony fishes. Immunogenetics 51 : 108 116.
53. von Schantz, T., Bensch, S., Grahn, M., Hasselquist, D. Wittzell, H. 1999. Good genes, oxidative stress and condition-dependent sexual signals. Proc. R. Soc. Lond. B 266 : 1 12.
54. Schaschl, H. Wegner, K.M. 2006. Polymorphism and signature of selection in the MHC class I genes of the three-spined stickleback (Gasterosteus aculeatus). J. Fish Biol. 69 (Suppl. B 177 188.
55. Schaschl, H. Wegner, K.M. 2007. Contrasting mode of evolution between the MHC class I genomic region and class II region in the three-spined stickleback (Gasterosteus aculeatus L.; Gasterosteidae: Teleostei). Immunogenetics 59 : 295 304.
56. Stearns, S.C. 1992. The Evolution of Life Histories. Oxford University Press, New York.
57. Stet, R.J.M., Kruiswijk, C.P. Dixon, B. 2003. Major histocompatibility lineages and immune gene function in teleost fish: the road not taken. Crit. Rev. Immunol. 23 : 441 471.
58. Wedekind, C., Seebeck, T., Bettens, F. Paepke, A.J. 1995. MHC-dependent mate preferences in humans. Proc. R. Soc. Lond. B 260 : 245 249.
59. Wegner, K.M. 2004. Major Histocompatibility Genes, Polymorphism and Balancing Selection - The Case of Parasites and Sticklebacks. PhD thesis. Christian-Albrechts-Universität, Kiel.
60. Wegner, K.M., Kalbe, M., Kurtz, J., Reusch, T.B.H. Milinski, M. 2003a. Parasite selection for immunogenetic optimality. Science 301 : 1343.
61. Wegner, K.M., Reusch, T.B.H. Kalbe, M. 2003b. Multiple parasites are driving major histocompatibility complex polymorphism in the wild. J. Evol. Biol. 16 : 224 232.
62. Wegner, K.M., Kalbe, M., Rauch, G., Kurtz, J., Schaschl, H. Reusch, T.B.H. 2006. Genetic variation in MHC class II expression and interactions with MHC sequence polymorphism in three-spined sticklebacks. Mol. Ecol. 15 : 1153 1164.
63. Wootton, R.J. 1976. The Biology of the Sticklebacks. Academic Press, New York.
64. Wootton, R.J. 1994. Energy allocation in the threespine stickleback. In : The Evolutionary Biology of the Threespine Stickleback (M. A. Bell S. A. Foster, eds pp. 114 143. Oxford University Press, New York.
65. 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 the major histocompatibility complex. J. Exp. Med. 144 : 1324 1335.
66. Zahavi, A. 1975. Mate selection - a selection for a handicap. J. Theor. Biol. 53 : 205 214.