Skip to main content
Log in

Ornamental comb colour predicts T-cell-mediated immunity in male red grouse Lagopus lagopus scoticus

  • Original Paper
  • Published:
Naturwissenschaften Aims and scope Submit manuscript

Abstract

Sexual ornaments might reliably indicate the ability to cope with parasites and diseases, and a better ability to mount a primary inflammatory response to a novel challenge. Carotenoid-based ornaments are amongst the commonest sexual signals of birds and often influence mate choice. Because carotenoids are immuno-stimulants, signallers may trade-off allocating these to ornamental colouration or using them for immune responses, so carotenoid-based ornaments might be particularly useful as honest indicators of immuno-compentence. Tetraonid birds, such as the red grouse Lagopus lagopus scoticus, exhibit supra-orbital yellow–red combs, a conspicuous ornament which functions in intra- and inter-sexual selection. The colour of combs is due to epidermal pigmentation by carotenoids, while their size is testosterone-dependent. In this study, I investigated whether comb characteristics, and in particular, comb colour, indicated immuno-competence in free-living male red grouse. I assessed T-cell-mediated immunity using a standardised challenge with phytohaemagglutinin. Red grouse combs reflect in the red and in the ultraviolet spectrum of light, which is not visible to humans but that grouse most likely see, so I measured comb colour across the whole bird visible spectrum (300–700 nm) using a reflectance spectrometer. I found that males with bigger and redder combs, but with less ultraviolet reflectance, had greater T-cell-mediated immune response. Comb colour predicted T-cell-mediated immune response better than comb size, indicating that the carotenoid-based colouration of this ornament might reliably signal this aspect of male quality.

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

Access this article

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

  • Alonso-Alvarez C, Bertrand S, Devevey G, Gaillard M, Prost J, Faivre B, Sorci G (2004) An experimental test of the dose-dependent effect of carotenoids and immune activation on sexual signals and antioxidant activity. Am Nat 164:651–659

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  • Bennett ATD, Cuthill IC, Partridge JC, Lunau K (1997) Ultraviolet plumage colors predict mate preferences in starlings. Proc Natl Acad Sci USA 94:8618–8621

    Article  PubMed  CAS  Google Scholar 

  • Blas J, Perez-Rodriguez L, Bortolotti GR, Vinuela J, Marchant TA (2006) Testosterone increases bioavailibility of carotenoids: insights into the honesty of sexual signalling. Proc Natl Acad Sci USA 103:18633–18637

    Article  PubMed  CAS  Google Scholar 

  • Cuthill IC, Bennett ATD, Partridge JC, Maier EJ (1999) Plumage reflectance and the objective assessment of avian sexual dichromatism. Am Nat 153:183–200

    Article  Google Scholar 

  • Duffy DL, Ball GF (2002) Song predicts immunocompetence in male European starlings (Sturnus vulgaris). Proc R Soc Lond B Biol Sci 269:847–852

    Article  Google Scholar 

  • Egeland ES, Parker H, Liaaenjensen S (1993) Carotenoids in combs of capercaillie (Tetrao urogallus) fed defined diets. Poultry Sci 72:747–751

    CAS  Google Scholar 

  • Endler JA (1990) On the measurement and classification of colour in studies of animal colour patterns. Biol J Linn Soc 41:315–352

    Google Scholar 

  • Faivre B, Gregoire A, Preault M, Cezilly F, Sorci G (2003a) Immune activation rapidly mirrored in a secondary sexual trait. Science 300:103

    Article  PubMed  CAS  Google Scholar 

  • Faivre B, Preault M, Salvadori F, Thery M, Gaillard M, Cezilly F (2003b) Bill colour and immunocompetence in the European blackbird. Anim Behav 65:1125–1131

    Article  Google Scholar 

  • Folstad I, Karter AJ (1992) Parasites, bright males, and the immunocompetence handicap. Am Nat 139:603–622

    Article  Google Scholar 

  • Getty T (2002) Signaling health versus parasites. Am Nat 159:363–371

    Article  PubMed  Google Scholar 

  • Goto N, Kodama H, Okada K, Fujimoto Y (1978) Suppression of phytohemagglutinin skin response in thymectomised chickens. Poultry Sci 57:246–250

    CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Hill GE (2002) A red bird in a brown bag: the function and evolution of ornamental plumage coloration in the house finch. Oxford University Press, Oxford

    Google Scholar 

  • Hill GE, McGraw KJ (2006) Avian coloration, vol 2: function and evolution. Harvard University Press, Cambridge

    Google Scholar 

  • Hollett KG, Thomas VG, MacDonald SD (1984) Structural and functional aspects of supraorbital combs of grouse. In: Hudson P, Lovel TWI (eds) Third international grouse symposium. World Pheasant Association, York, pp 193–211

    Google Scholar 

  • Hudson PJ (1986) The red grouse: the biology and management of a wild gamebird. The Game Conservancy Trust, Fordingbridge

    Google Scholar 

  • Kennedy MW, Nager RG (2006) The perils and prospects of using phytohaemagglutinin in evolutionary ecology. Trends Ecol Evol 21:653–655

    Article  PubMed  Google Scholar 

  • Martin LB, Han P, Lewittes J, Kuhlman JR, Klasing KC, Wikelski M (2006) Phytohemagglutinin-induced skin swelling in birds: histological support for a classic immunoecological technique. Funct Ecol 20:290–299

    Article  Google Scholar 

  • Martinez-Padilla J (2006) Daytime variation in T-cell-mediated immunity of Eurasian kestrel Falco tinnunculus nestlings. J Avian Biol 37:419–424

    Article  Google Scholar 

  • Martinez-Padilla J, Mougeot F, Perez-Rodriguez L, Bortolotti GR (2007) Nematode parasites reduce carotenoid-based signalling in male red grouse. Biol Lett 3:161–164

    Article  PubMed  CAS  Google Scholar 

  • McGraw KJ (2006) The mechanics of carotenoid coloration in birds. In: Hill GE, McGraw KJ (eds) Bird coloration. I. Mechanisms and measurements, vol I. Harvard University Press, Cambridge

    Google Scholar 

  • McGraw KJ, Ardia DR (2003) Carotenoids, immunocompetence, and the information content of sexual colors: an experimental test. Am Nat 162:704–712

    Article  PubMed  Google Scholar 

  • Møller AP (1990) Parasites and sexual selection—current status of the Hamilton and Zuk hypothesis. J Evol Biol 3:319–328

    Article  Google Scholar 

  • Møller AP, Saino N (1994) Parasites, immunology of hosts, and host sexual selection. J Parasitol 80:850–858

    Article  PubMed  Google Scholar 

  • Møller AP, Dufva R, Erritzoe J (1998) Host immune function and sexual selection in birds. J Evol Biol 11:703–719

    Article  Google Scholar 

  • Møller AP, Christe P, Lux E (1999) Parasitism, host immune function, and sexual selection. Q Rev Biol 74:3–20

    Article  PubMed  Google Scholar 

  • Møller AP, Biard C, Blount JD, Houston DC, Ninni P, Saino N, Surai PF (2000) Carotenoid-dependent signals: indicators of foraging efficiency, immunocompetence or detoxification ability? Avian Poult Biol Rev 11:137–159

    Google Scholar 

  • Moss R, Kolb HH, Marquiss M, Watson A, Treca B, Watt D, Glennie W (1979) Aggressiveness and dominance in captive cock red grouse. Aggress Behav 5:58–84

    Article  Google Scholar 

  • Mougeot F, Redpath S (2004) Sexual ornamentation relates to immune function in male red grouse Lagopus lagopus scoticus. J Avian Biol 35:425–433

    Article  Google Scholar 

  • Mougeot F, Irvine J, Seivwright LJ, Redpath S, Piertney SB (2004) Testosterone, immunocompetence and honest sexual signaling in male red grouse. Behav Ecol 15:630–637

    Article  Google Scholar 

  • Mougeot F, Dawson A, Redpath S, Leckie F (2005a) Testosterone and autumn territorial behaviour in male red grouse Lagopus lagopus scoticus. Horm Behav 47:576–584

    Article  PubMed  CAS  Google Scholar 

  • Mougeot F, Evans S, Redpath S (2005b) Interactions between population processes in a cyclic species: parasites reduce autumn territorial behaviour in male red grouse. Oecologia 144:289–298

    Article  PubMed  Google Scholar 

  • Mougeot F, Martinez-Padilla J, Pérez-Rodríguez L, Bortolotti GR (2007a) Carotenoid-based coloration and ultraviolet reflectance of the sexual ornaments of grouse. Behav Ecol Sociobiol 61:741–751

    Article  Google Scholar 

  • Mougeot F, Perez-Rodriguez L, Martinez-Padilla J, Leckie F, Redpath SM (2007b) Parasites, testosterone and honest carotenoid-based signalling of health. Funct Ecol 21:886–898

    Article  Google Scholar 

  • Olson VA, Owens IPF (1998) Costly sexual signals: are carotenoids rare, risky or required? Trends Ecol Evol 13:510–514

    Article  Google Scholar 

  • Peters A, Denk AG, Delhey AG, Kempenaers B (2004) Carotenoid-based bill colour as an indicator of immunocompetence and sperm performance in male mallards. J Evol Biol 17:1111–1120

    Article  PubMed  CAS  Google Scholar 

  • Redpath S, Mougeot F, Leckie F, Evans S (2006) The effects of autumn testosterone on survival and productivity in red grouse Lagopus lagopus scoticus. Anim Behav 71:1297–1305

    Article  Google Scholar 

  • Saino N, Bolzern AM, Møller AP (1997) Immunocompetence, ornamentation and viability of male barn swallows (Hirundo rustica). Proc Natl Acad Sci USA 94:549–552

    Article  PubMed  CAS  Google Scholar 

  • SAS (2001) SAS/STAT user’s guide, version 8.01. SAS Insitute, Cary

    Google Scholar 

  • Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol 11:317–321

    Article  Google Scholar 

  • Siitari H, Viitala J (2002) Behavioural evidence for ultraviolet vision in a tetraonid species foraging experiment with black grouse Tetrao tetrix. J Avian Biol 33:199–202

    Article  Google Scholar 

  • Smith SE, Bortolotti GR, Tella JL (1999) Simplifying the phytohaemagglutinin skin-testing technique in studies of avian immunocompetence. Funct Ecol 13:567–572

    Article  CAS  Google Scholar 

  • 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 Biol Sci 266:1–12

    Article  Google Scholar 

  • Zahavi A, Zahavi A (1997) The Handicap Principle: a missing piece of Darwin’s puzzle. University Press, Oxford

    Google Scholar 

  • Zuk M (1992) The role of parasites in sexual selection—current evidence and future directions. Adv Study Behav 21:39–68

    Article  Google Scholar 

  • Zuk M (1996) Disease, endocrine-immune interactions, and sexual selection. Ecology 77:1037–1042

    Article  Google Scholar 

  • Zuk M, Johnsen TS, Maclarty T (1995) Endocrine-immune interactions, ornaments and mate choice in red jungle fowl. Proc R Soc Lond B Biol Sci 260:205–210

    Article  Google Scholar 

Download references

Acknowledgements

I am grateful to the owner and gamekeepers of the Edinglassie estate (Aberdeenshire, north-east Scotland) for allowing me to conduct this work on their grouse moors. Special thanks are due to Derek Calder (headkeeper) for his help with organising the work. I also thank F. Leckie and J. Irvine for their help with the fieldwork, M. Evans for providing advice and material for the immune challenges and J. Martinez-Padilla and L. Perez-Rodriguez for helpful comments on an earlier version of the manuscript. All procedures were conducted under a UK Home Office licence (PPL 80/1437). I was supported by a National Environmental Research Council (NERC) fellowship and a Grant from the Ministerio de Educacion y Ciencia, Spain (CGL 2006-11823).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Francois Mougeot.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mougeot, F. Ornamental comb colour predicts T-cell-mediated immunity in male red grouse Lagopus lagopus scoticus . Naturwissenschaften 95, 125–132 (2008). https://doi.org/10.1007/s00114-007-0303-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00114-007-0303-6

Keywords

Navigation