Skip to main content
SpringerLink
Log in

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

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • 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):133–142

    Article  CAS  PubMed  Google Scholar 

  • Andersson M (1994) Sexual selection. Princeton University Press, Princeton

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Bollmer JL, Vargas FH, Parker PG (2007) Low MHC variation in the endangered Galapagos penguin (Spheniscus mendiculus). Immunogenetics 59(7):593–602

    Article  CAS  PubMed  Google Scholar 

  • 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):171–178

    Google Scholar 

  • 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 121:176–185

    Article  Google Scholar 

  • Danchin EG, Pontarotti P (2004) Towards the reconstruction of the bilaterian ancestral pre-MHC region. Trend Gen 20(12):587–591

    Article  CAS  Google Scholar 

  • Dawkins R (1976) The selfish gene. Oxford University Press, Oxford

    Google Scholar 

  • 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 55:616–625

    Article  CAS  PubMed  Google Scholar 

  • 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 16:1439–1451

    Article  PubMed  Google Scholar 

  • Grafen A (1990) Biological signals as handicaps. J Theor Biol 144(4):517–546

    Article  CAS  PubMed  Google Scholar 

  • Grahn M, von Schantz T (1994) Fashion and age in pheasants: age differences in mate choice. P Roy Soc B-Biol Sci 255:237–241

    Article  Google Scholar 

  • 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 7:2775–2785

    CAS  PubMed  Google Scholar 

  • 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):1284–1294

    Article  CAS  Google Scholar 

  • Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds: a role for parasites? Science 218:384–387

    Article  CAS  PubMed  Google Scholar 

  • Hedrick PW (1999) Perspective: highly variable genetic loci and their interpretation in evolution and conservation. Evolution 53:313–318

    Article  Google Scholar 

  • Hedrick PW, Parker K, Miller EL, Miller PS (1999) Major histocompatibility complex variation in the endangered Przewalski’s horse. Genetics 152:1701–1710

    CAS  PubMed  Google Scholar 

  • Hedrick PW, Parker KM, Gutierrez-Espleta G, Rattink A, Lievers K (2000) Major histocompatibility complex variation in the Arabian oryx. Evolution 54(6):2145–2151

    CAS  PubMed  Google Scholar 

  • Hedrick PW, Kim TJ, Parker KM (2001) Parasite resistance and genetic variation in the endangered Gila topminnow. Anim Conserv 4:103–109

    Article  Google Scholar 

  • Hillgarth N (1990) Parasite and female choice in the ring-necked pheasant. Amer Zool 30(2):227–233

    Google Scholar 

  • 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):611–618

    CAS  PubMed  Google Scholar 

  • Hosmer DW, Lemeshow S (1989) Applied logistic regression. Wiley, New York

    Google Scholar 

  • Hunt J, Bussiere L, Jennions MD, Brooks RC (2004) What is genetic quality? Trends Ecol Evol 19:329–333

    Article  PubMed  Google Scholar 

  • 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):2005–2015

    Article  PubMed  Google Scholar 

  • Janetos AC, Cole BJ (1981) Imperfectly optimal animals. Behav Ecol Sociobiol 9(3):203–209

    Article  Google Scholar 

  • Jarvi SI, Briles WE (1992) Identification of the major histocompatibility complex in the ring-necked pheasant, Phasianus colchicus. Anim Gen 23(3):211–220

    Article  CAS  Google Scholar 

  • Jarvi SI, Goto RM, Briles WE, Miller MM (1996) Characterization of MHC genes in a multigenerational family of ring-necked pheasants. Immunogenetics 43(3):125–135

    Article  CAS  PubMed  Google Scholar 

  • Johnsgard PA (1999) The quails partridges, and francolins of the world. Oxford University Press, Oxford

    Google Scholar 

  • 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):651–658

    Article  PubMed  Google Scholar 

  • Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HM (ed) Mammalian protein metabolism. Academic Press, New York, pp 21–132

    Google Scholar 

  • 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 25:105–111

    Article  CAS  PubMed  Google Scholar 

  • Kelley J, Walter L, Trowsdale J (2005) Comparative genomics of major histocompatibility complexes. Immunogenetics 56:683–695

    Article  CAS  PubMed  Google Scholar 

  • Kellner JR, Alford RA (2003) The ontogeny of fluctuating asymmetry. Am Nat 161:931–947

    Article  PubMed  Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16(2):111–120

    Article  CAS  PubMed  Google Scholar 

  • Klein J (1986) Natural history of the major histocompatibility complex. Wiley, New York

    Google Scholar 

  • Kourkine IV, Hestekin CN, Barron AE (2002) Technical challenges in applying capillary electrophoresis-single strand conformation polymorphism for routine genetic analysis. Electrophoresis 23:1375–1385

    Article  CAS  PubMed  Google Scholar 

  • Kroemer G, Guillemot F, Auffray C (1990) Genetic organization of the chicken MHC. Immunol Res 9(1):8–19

    Article  CAS  PubMed  Google Scholar 

  • Kumar S, Tamura K, Masatoshi N (2004) MEGA 3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5(2):150–163

    Article  CAS  PubMed  Google Scholar 

  • Leamy LJ, Klingenberg CP (2005) The genetics and evolution of fluctuating asymmetry. Annu Rev Ecol Evol Syst 36:1–21

    Article  Google Scholar 

  • Lehmann L, Keller LF, Kokko H (2007) Mate choice evolution, dominance effects and the maintenance of genetic variation. J Theor Biol 244:282–295

    Article  CAS  PubMed  Google Scholar 

  • Longeri M, Zanotti M, Damiani G (2002) Recombinant DRB sequences produced by mismatch repair of heteroduplexes during cloning in Escherichia coli. Eur J Immunogenet 29:517–523

    Article  CAS  PubMed  Google Scholar 

  • Mays HL Jr, Hill GE (2004) Choosing mates: good genes versus genes that are a good fit. Trends Ecol Evol 19(10):554–559

    Article  PubMed  Google Scholar 

  • Mays HL Jr, Albrecht T, Liu M, Hill GE (2008) Female choice for genetic complementarity in birds: a review. Genetica 134(1):147–158

    Article  PubMed  Google Scholar 

  • Milinski M (2006) The major histocompatibility complex, sexual selection and mate choice. Annu Rev Ecol Evol Syst 37:159–186

    Article  Google Scholar 

  • Mǿller AP (1992) Female swallow preference for symmetrical male sexual ornaments. Nature 357(6375):238–240

    Article  PubMed  Google Scholar 

  • Mǿller AP (1999) Developmental stability is related to fitness. Am Nat 153(5):556–560

    Article  Google Scholar 

  • Mǿller AP (2006) A review of developmental instability, parasitism and disease infection, genetics and evolution. Infect Genet Evol 6(2):133–140

    Article  PubMed  Google Scholar 

  • Nagelkerke NJD (1991) A note on the general definition of the coefficient of determination. Biometrika 78(3):691–692

    Article  Google Scholar 

  • Neff BD, Pitcher TE (2005) Genetic quality and sexual selection: an integrated framework for good genes and compatible genes. Mol Ecol 14:19–38

    Article  CAS  PubMed  Google Scholar 

  • Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3:418–426

    CAS  PubMed  Google Scholar 

  • Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New York

    Google Scholar 

  • Ohlsson T, Smith HG, Råberg L, Hasselquist D (2002) Pheasant sexual ornaments reflect nutritional conditions during early growth. P Roy Soc B-Biol Sci 269:21–27

    Article  Google Scholar 

  • 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):390–395

    Article  CAS  PubMed  Google Scholar 

  • 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 191:55–70

    Google Scholar 

  • Papeschi A (1998) Ornamenti maschili e selezione sessuale nel fagiano commune (Phasianus colchicus). PhD dissertation, University of Florence

  • Papeschi A, Dessi-Fulgheri F (2003) Multiple ornaments are positively related to male survival in the common pheasant. Anim Behav 65:143–147

    Article  Google Scholar 

  • Papeschi A, Briganti F, Dessi-Fulgheri F (2000) Winter androgen levels and wattle size in male common pheasants. Condor 102(1):193–197

    Article  Google Scholar 

  • Penn DJ (2002) The scent of genetic compatibility: sexual selection and the major histocompatibility complex. Ethology 108:1–21

    Article  Google Scholar 

  • Piertney SB, Oliver MK (2006) The evolutionary ecology of the major histocompatibility complex. J Hered 96:7–21

    CAS  Google Scholar 

  • Polak M, Taylor PW (2007) A primary role of developmental instability in sexual selection. P Roy Soc B-Biol Sci 274:3133–3140

    Article  Google Scholar 

  • Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14(9):817–818

    Article  CAS  PubMed  Google Scholar 

  • Radwan J (2008) Maintenance of genetic variation in sexual ornaments: a review of the mechanisms. Genetica 134(1):113–127

    Article  PubMed  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  CAS  PubMed  Google Scholar 

  • Searle SR (1982) Matrix algebra useful for statistics. Wiley, New York

    Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry. The principles and practice of statistics in biological research, 3rd edn. W.H Freeman and co, New York

    Google Scholar 

  • Sommer S (2005) The importance of immune gene variability (MHC) in evolutionary ecology and conservation. Front Zool 20(2):16

    Article  CAS  Google Scholar 

  • 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 59:725–734

    Article  CAS  PubMed  Google Scholar 

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    CAS  PubMed  Google Scholar 

  • 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 25:4876–4882

    Article  CAS  Google Scholar 

  • Trowsdale J, Parham P (2004) Mini-review: defense strategies and immunity-related genes. Eur J Immunol 34:7–17

    Article  CAS  PubMed  Google Scholar 

  • 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):1679–1688

    Article  PubMed  Google Scholar 

  • van Oosterhout C, Joyce DA, Cummings SM (2006) Evolution of MHC class IIB in the genome of wild and ornamental guppies, Poecilia reticulata. Heredity 97:111–118

    Article  PubMed  CAS  Google Scholar 

  • 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):265–271

    Article  Google Scholar 

  • 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):133–140

    Article  Google Scholar 

  • Westerdahl H, Wittzell H, von Schantz T (2000) MHC diversity in two passerine birds: no evidence for a minimal essential MHC. Immunogenetics 52:92–100

    Article  CAS  PubMed  Google Scholar 

  • 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 39:395–403

    Article  CAS  PubMed  Google Scholar 

  • Wittzell H, Madsen T, Westerdahl H, Shine R, von Schantz T (1998) MHC variation in birds and reptiles. Genetica 104(3):301–309

    Article  CAS  PubMed  Google Scholar 

  • 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):479–490

    CAS  PubMed  Google Scholar 

  • Zahavi A (1975) Mate selection: a selection for a handicap. J Theor Biol 53:205–214

    Article  CAS  PubMed  Google Scholar 

  • 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):110–120

    Article  CAS  Google Scholar 

Download references

Acknowledgments

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.

Author information

Authors and Affiliations

  1. Institute for Ecosystem Study, C.N.R., Via Madonna del Piano 10, 50019, Sesto Fiorentino (Firenze), Italy

    Mariella Baratti

  2. Department of Evolutionary Biology “L. Pardi”, University of Florence, Via Romana 17, 50125, Florence, Italy

    Martina Ammannati, Claudia Magnelli & Francesco Dessì-Fulgheri

  3. Department of Ecosystem and Public Health, Faculty of Veterinary Medicine, University of Calgary, Calgary, AB, Canada

    Alessandro Massolo

Authors
  1. Mariella Baratti
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Martina Ammannati
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Claudia Magnelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Alessandro Massolo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Francesco Dessì-Fulgheri
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mariella Baratti.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Baratti, M., Ammannati, M., Magnelli, C. et al. Are large wattles related to particular MHC genotypes in the male pheasant?. Genetica 138, 657–665 (2010). https://doi.org/10.1007/s10709-010-9440-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10709-010-9440-5

Keywords

Search

Navigation