, Volume 138, Issue 6, pp 657–665 | Cite as

Are large wattles related to particular MHC genotypes in the male pheasant?

  • Mariella BarattiEmail author
  • Martina Ammannati
  • Claudia Magnelli
  • Alessandro Massolo
  • Francesco Dessì-Fulgheri


In sexually dimorphic species, partners can assess heritable mate quality by analyzing costly sexual ornaments in terms of their dimension and possibly of their symmetry. In vertebrates an important aspect of genetic quality is the efficiency of the immune system, and in particular the Major Histocompatibility Complex (MHC). If ornaments are honest advertisements of pathogen resistance (good genes), in line with the Hamilton-Zuk hypothesis, a correlation between ornament expression and MHC profiles should exist. We tested this hypothesis in the common pheasant Phasianus colchicus by comparing male ornament characteristics (wattle and spur size, and wattle fluctuating asymmetry) with a portion of exon 2 of the class IIB MHC genes containing 19 putative antigen recognition sites. A total of 8 new alleles was observed in the MHCPhco exon IIB. We found significant differences in the occurrence of MHC genotypes between males carrying large or small wattles. Homozygous genotypes predicted large wattle males more correctly than small wattle males. The association between the dimension of the spur and the occurrence of MHC genotypes was marginally significant, however, we did not find any significant association between MHC genotypes and asymmetry. Our results suggest that female pheasants may use the ornament size as a cue to evaluate male quality and thus choose males carrying particular MHC profiles.


CE-SSCP Good genes Hamilton-Zuk hypothesis MHC Ornaments Symmetry 



We thank R. Stanyon, G. Bertorelle, M. Ciuffreda and S. Mona for comments and suggestions. We thanks the CIBIACI sequencing centre for optimizing the CE-SSCP technique. This research was supported by grants from the Italian Ministry (PRIN/2005). We also thank G. Sanders for English revision.


  1. Aguilar A, Edwards SV, Smith TB, Wayne RK (2006) Patterns of variation in MHC class II b loci of the little greenbul (Andropadus virens) with comments on MHC evolution in birds. J Hered 97(2):133–142CrossRefPubMedGoogle Scholar
  2. Andersson M (1994) Sexual selection. Princeton University Press, PrincetonGoogle Scholar
  3. Bernatchez L, Landry C (2003) MHC studies in nonmodel vertebrates: what have we learned about natural selection in 15 years? J Evol Biol 16:363–377CrossRefPubMedGoogle Scholar
  4. Bollmer JL, Vargas FH, Parker PG (2007) Low MHC variation in the endangered Galapagos penguin (Spheniscus mendiculus). Immunogenetics 59(7):593–602CrossRefPubMedGoogle Scholar
  5. Briganti F, Papeschi A, Mugnai T, Dessì-Fulgheri F (1999) Effect of testosterone on male traits and behaviour in juvenile pheasants. Ethol Ecol Evol 11(2):171–178Google Scholar
  6. Buchholz R, Jones Dukes MD, Hecht SJ, Findley AM (2004) Investigating the turkey’s “snood” asa morphological marker of heritable disease resistance. J Anim Breed Genet 121:176–185CrossRefGoogle Scholar
  7. Danchin EG, Pontarotti P (2004) Towards the reconstruction of the bilaterian ancestral pre-MHC region. Trend Gen 20(12):587–591CrossRefGoogle Scholar
  8. Dawkins R (1976) The selfish gene. Oxford University Press, OxfordGoogle Scholar
  9. Ditchkoff SS, Lochmiller RL, Masters RE, Hoofer SR, van den Bussche RA (2001) Major-histocompatibility-complex-associated variation in secondary sexual traits of whitetailed deer (Odocoileus virginianus): evidence for good-genes advertisement. Evolution 55:616–625CrossRefPubMedGoogle Scholar
  10. Ekblom R, Saether SA, Jacobsson P, Fiske P, Sahlman T, Grahn M, Kålås JA, Höglund J (2007) Spatial pattern of MHC class II variation in the great snipe (Gallinago media). Mol Ecol 16:1439–1451CrossRefPubMedGoogle Scholar
  11. Grafen A (1990) Biological signals as handicaps. J Theor Biol 144(4):517–546CrossRefPubMedGoogle Scholar
  12. Grahn M, von Schantz T (1994) Fashion and age in pheasants: age differences in mate choice. P Roy Soc B-Biol Sci 255:237–241CrossRefGoogle Scholar
  13. Guillemot F, Billault A, Pourquie O, Behar G, Chausse AM, Zoorob R, Kreibich G, Auffray C (1988) A molecular map of the chicken major histocompatibility complex: the class II beta genes are closely linked to the class I genes and the nucleolar organizer. EMBO J 7:2775–2785PubMedGoogle Scholar
  14. Hale ML, Verduijn MH, Moller AP, Wolff K, Petrie MS (2009) Is the peacock’s train an honest signal of genetic quality at the major histocompatibility complex? J Evolution Biol 22(6):1284–1294CrossRefGoogle Scholar
  15. Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds: a role for parasites? Science 218:384–387CrossRefPubMedGoogle Scholar
  16. Hedrick PW (1999) Perspective: highly variable genetic loci and their interpretation in evolution and conservation. Evolution 53:313–318CrossRefGoogle Scholar
  17. Hedrick PW, Parker K, Miller EL, Miller PS (1999) Major histocompatibility complex variation in the endangered Przewalski’s horse. Genetics 152:1701–1710PubMedGoogle Scholar
  18. Hedrick PW, Parker KM, Gutierrez-Espleta G, Rattink A, Lievers K (2000) Major histocompatibility complex variation in the Arabian oryx. Evolution 54(6):2145–2151PubMedGoogle Scholar
  19. Hedrick PW, Kim TJ, Parker KM (2001) Parasite resistance and genetic variation in the endangered Gila topminnow. Anim Conserv 4:103–109CrossRefGoogle Scholar
  20. Hillgarth N (1990) Parasite and female choice in the ring-necked pheasant. Amer Zool 30(2):227–233Google Scholar
  21. Hoelzel AR, Stephens JC, O’Brien SJ (1999) Molecular genetic diversity and evolution at the MHC DQB locus in four species of pinnipeds. Mol Biol Evol 16(5):611–618PubMedGoogle Scholar
  22. Hosmer DW, Lemeshow S (1989) Applied logistic regression. Wiley, New YorkGoogle Scholar
  23. Hunt J, Bussiere L, Jennions MD, Brooks RC (2004) What is genetic quality? Trends Ecol Evol 19:329–333CrossRefPubMedGoogle Scholar
  24. Jäger I, Eizaguirre C, Griffiths SW, Kalbe M, Krobbach CK, Reusch TB, Schaschl H, Milinski M (2007) Individual MHC class I and MHC class IIB diversities are associated with male and female reproductive traits in the three-spined stickleback. J Evol Biol 20(5):2005–2015CrossRefPubMedGoogle Scholar
  25. Janetos AC, Cole BJ (1981) Imperfectly optimal animals. Behav Ecol Sociobiol 9(3):203–209CrossRefGoogle Scholar
  26. Jarvi SI, Briles WE (1992) Identification of the major histocompatibility complex in the ring-necked pheasant, Phasianus colchicus. Anim Gen 23(3):211–220CrossRefGoogle Scholar
  27. Jarvi SI, Goto RM, Briles WE, Miller MM (1996) Characterization of MHC genes in a multigenerational family of ring-necked pheasants. Immunogenetics 43(3):125–135CrossRefPubMedGoogle Scholar
  28. Johnsgard PA (1999) The quails partridges, and francolins of the world. Oxford University Press, OxfordGoogle Scholar
  29. Johnson W, Gangestad SW, Segal NL, Bouchard TJ Jr (2008) Heritability of fluctuating asymmetry in a human twin sample: the effect of trait aggregation. Am J Hum Biol 20(6):651–658CrossRefPubMedGoogle Scholar
  30. Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HM (ed) Mammalian protein metabolism. Academic Press, New York, pp 21–132Google Scholar
  31. Kasahara M, Suzuki T, Du Pasquier L (2004) On the origins of the adaptive immune system: novel insights from invertebrates and cold-blooded vertebrates. Trends Immunol 25:105–111CrossRefPubMedGoogle Scholar
  32. Kelley J, Walter L, Trowsdale J (2005) Comparative genomics of major histocompatibility complexes. Immunogenetics 56:683–695CrossRefPubMedGoogle Scholar
  33. Kellner JR, Alford RA (2003) The ontogeny of fluctuating asymmetry. Am Nat 161:931–947CrossRefPubMedGoogle Scholar
  34. Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16(2):111–120CrossRefPubMedGoogle Scholar
  35. Klein J (1986) Natural history of the major histocompatibility complex. Wiley, New YorkGoogle Scholar
  36. Kourkine IV, Hestekin CN, Barron AE (2002) Technical challenges in applying capillary electrophoresis-single strand conformation polymorphism for routine genetic analysis. Electrophoresis 23:1375–1385CrossRefPubMedGoogle Scholar
  37. Kroemer G, Guillemot F, Auffray C (1990) Genetic organization of the chicken MHC. Immunol Res 9(1):8–19CrossRefPubMedGoogle Scholar
  38. Kumar S, Tamura K, Masatoshi N (2004) MEGA 3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5(2):150–163CrossRefPubMedGoogle Scholar
  39. Leamy LJ, Klingenberg CP (2005) The genetics and evolution of fluctuating asymmetry. Annu Rev Ecol Evol Syst 36:1–21CrossRefGoogle Scholar
  40. Lehmann L, Keller LF, Kokko H (2007) Mate choice evolution, dominance effects and the maintenance of genetic variation. J Theor Biol 244:282–295CrossRefPubMedGoogle Scholar
  41. Longeri M, Zanotti M, Damiani G (2002) Recombinant DRB sequences produced by mismatch repair of heteroduplexes during cloning in Escherichia coli. Eur J Immunogenet 29:517–523CrossRefPubMedGoogle Scholar
  42. Mays HL Jr, Hill GE (2004) Choosing mates: good genes versus genes that are a good fit. Trends Ecol Evol 19(10):554–559CrossRefPubMedGoogle Scholar
  43. Mays HL Jr, Albrecht T, Liu M, Hill GE (2008) Female choice for genetic complementarity in birds: a review. Genetica 134(1):147–158CrossRefPubMedGoogle Scholar
  44. Milinski M (2006) The major histocompatibility complex, sexual selection and mate choice. Annu Rev Ecol Evol Syst 37:159–186CrossRefGoogle Scholar
  45. Mǿller AP (1992) Female swallow preference for symmetrical male sexual ornaments. Nature 357(6375):238–240CrossRefPubMedGoogle Scholar
  46. Mǿller AP (1999) Developmental stability is related to fitness. Am Nat 153(5):556–560CrossRefGoogle Scholar
  47. Mǿller AP (2006) A review of developmental instability, parasitism and disease infection, genetics and evolution. Infect Genet Evol 6(2):133–140CrossRefPubMedGoogle Scholar
  48. Nagelkerke NJD (1991) A note on the general definition of the coefficient of determination. Biometrika 78(3):691–692CrossRefGoogle Scholar
  49. Neff BD, Pitcher TE (2005) Genetic quality and sexual selection: an integrated framework for good genes and compatible genes. Mol Ecol 14:19–38CrossRefPubMedGoogle Scholar
  50. Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3:418–426PubMedGoogle Scholar
  51. Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New YorkGoogle Scholar
  52. Ohlsson T, Smith HG, Råberg L, Hasselquist D (2002) Pheasant sexual ornaments reflect nutritional conditions during early growth. P Roy Soc B-Biol Sci 269:21–27CrossRefGoogle Scholar
  53. Oliver MK, Piertney SB (2006) Isolation and characterization of a MHC class II DRB locus in the European water vole (Arvicola terrestris). Immunogenetics 58(5–6):390–395CrossRefPubMedGoogle Scholar
  54. Palmer AR, Strobeck C (1992) Fluctuating asymmetry as a measure of developmental stability: implications of non-normal distributions and power of statistical tests. Acta Zool Fenn 191:55–70Google Scholar
  55. Papeschi A (1998) Ornamenti maschili e selezione sessuale nel fagiano commune (Phasianus colchicus). PhD dissertation, University of FlorenceGoogle Scholar
  56. Papeschi A, Dessi-Fulgheri F (2003) Multiple ornaments are positively related to male survival in the common pheasant. Anim Behav 65:143–147CrossRefGoogle Scholar
  57. Papeschi A, Briganti F, Dessi-Fulgheri F (2000) Winter androgen levels and wattle size in male common pheasants. Condor 102(1):193–197CrossRefGoogle Scholar
  58. Penn DJ (2002) The scent of genetic compatibility: sexual selection and the major histocompatibility complex. Ethology 108:1–21CrossRefGoogle Scholar
  59. Piertney SB, Oliver MK (2006) The evolutionary ecology of the major histocompatibility complex. J Hered 96:7–21Google Scholar
  60. Polak M, Taylor PW (2007) A primary role of developmental instability in sexual selection. P Roy Soc B-Biol Sci 274:3133–3140CrossRefGoogle Scholar
  61. Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14(9):817–818CrossRefPubMedGoogle Scholar
  62. Radwan J (2008) Maintenance of genetic variation in sexual ornaments: a review of the mechanisms. Genetica 134(1):113–127CrossRefPubMedGoogle Scholar
  63. Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574CrossRefPubMedGoogle Scholar
  64. Searle SR (1982) Matrix algebra useful for statistics. Wiley, New YorkGoogle Scholar
  65. Sokal RR, Rohlf FJ (1995) Biometry. The principles and practice of statistics in biological research, 3rd edn. W.H Freeman and co, New YorkGoogle Scholar
  66. Sommer S (2005) The importance of immune gene variability (MHC) in evolutionary ecology and conservation. Front Zool 20(2):16CrossRefGoogle Scholar
  67. Strand T, Westerdahl H, Höglund J, Alatalo RV, Siitari H (2007) The Mhc class II of the Black grouse (Tetrao tetrix) consists of low numbers of B and Y genes with variable diversity and expression. Immunogenetics 59:725–734CrossRefPubMedGoogle Scholar
  68. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595PubMedGoogle Scholar
  69. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequenze alignment aided by quality analysis tools. Nuc Acid Res 25:4876–4882CrossRefGoogle Scholar
  70. Trowsdale J, Parham P (2004) Mini-review: defense strategies and immunity-related genes. Eur J Immunol 34:7–17CrossRefPubMedGoogle Scholar
  71. Van der Walt M, Nel LH, Hoelzel AR (2001) Characterization of major histocompatibility complex DRB diversity in the endemic South African antelope Damaliscus pygargus: a comparison in two subspecies with different demographic histories. Mol Ecol 10(7):1679–1688CrossRefPubMedGoogle Scholar
  72. van Oosterhout C, Joyce DA, Cummings SM (2006) Evolution of MHC class IIB in the genome of wild and ornamental guppies, Poecilia reticulata. Heredity 97:111–118CrossRefPubMedGoogle Scholar
  73. von Schantz T, Wittzell H, Goransson G, Grahn M, Persson K (1996) MHC genotype and male ornamentation: genetic evidence for the Hamilton-Zuk model. Proc R Soc B-Biol Sci 263(1368):265–271CrossRefGoogle Scholar
  74. von Schantz T, Wittzell H, Goransson G, Grahn M (1997) Mate choice, male condition-dependent ornamentation and MHC in the pheasant. Hereditas 127(1–2):133–140CrossRefGoogle Scholar
  75. Westerdahl H, Wittzell H, von Schantz T (2000) MHC diversity in two passerine birds: no evidence for a minimal essential MHC. Immunogenetics 52:92–100CrossRefPubMedGoogle Scholar
  76. Wittzell H, von Schantz T, Zoorob R, Auffray C (1994) Molecular characterization of three MHC class II B haplotypes in the ring-necked pheasant. Immunogenetics 39:395–403CrossRefPubMedGoogle Scholar
  77. Wittzell H, Madsen T, Westerdahl H, Shine R, von Schantz T (1998) MHC variation in birds and reptiles. Genetica 104(3):301–309CrossRefPubMedGoogle Scholar
  78. Wittzell H, Bernot A, Auffray C, Zoorob R (1999) Concerted evolution of two MHC class II B loci in pheasants and domestic chickens. Mol Biol Evol 16(4):479–490PubMedGoogle Scholar
  79. Zahavi A (1975) Mate selection: a selection for a handicap. J Theor Biol 53:205–214CrossRefPubMedGoogle Scholar
  80. Zhang B, Fang SG, Xi YM (2006) Major histocompatibility complex variation in the endangered crested ibis Nipponia nippon and implications for reintroduction. Biochem Genet 44(3):110–120CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Mariella Baratti
    • 1
    Email author
  • Martina Ammannati
    • 2
  • Claudia Magnelli
    • 2
  • Alessandro Massolo
    • 3
  • Francesco Dessì-Fulgheri
    • 2
  1. 1.Institute for Ecosystem Study, C.N.R.Sesto Fiorentino (Firenze)Italy
  2. 2.Department of Evolutionary Biology “L. Pardi”University of FlorenceFlorenceItaly
  3. 3.Department of Ecosystem and Public Health, Faculty of Veterinary MedicineUniversity of CalgaryCalgaryCanada

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