Naturwissenschaften

, Volume 94, Issue 11, pp 895–902

Carotenoids, immune response and the expression of sexual ornaments in male greenfinches (Carduelis chloris)

Original Paper

Abstract

Allocation trade-offs of carotenoids between their use in the immune system and production of sexual ornaments have been suggested as a proximate mechanism maintaining honesty of sexual signals. To test this idea, we experimentally examined whether carotenoid availability in the diet was related to variation in antibody response to novel antigens in male greenfinches (Carduelis chloris aurantiiventris), a species with extensive carotenoid-dependent plumage colouration. We also measured the cost of mounting a humoral response in terms of circulating carotenoids. Finally, we examined the relationship between plumage colour, immune response and circulating carotenoids. We found that males with carotenoid-supplemented diets showed stronger antibody response than non-supplemented birds. We also found that activation of the immune system significantly reduced circulating carotenoids (24.9% lower in immune-challenged birds than in control birds). Finally, intensity (chroma) of ventral plumage colouration of males, a character directly related to concentration of total carotenoids in feathers, was negatively correlated with the immune response and circulating carotenoids in winter. These results support the idea that carotenoids are a limiting resource and that males trade ornamental colouration against immune response.

Keywords

Sexual selection Immune response Carotenoids Plumage colour 

References

  1. Allen PT (1987) Effect of Eimeria acervulina infection on chick (Gallus domesticus) high density lipoprotein composition. Comp Biochem Physiol 87B:313–319Google Scholar
  2. Allen PT (1992) Effect of coccidiosis on the distribution of dietary lutein in the chick. Poult Sci 71:1457–1463PubMedGoogle Scholar
  3. 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 164:651–659PubMedCrossRefGoogle Scholar
  4. Amat JA, Aguilera E, Visser GH (2007) Energetic and developmental costs of mounting an immune response in greenfinches (Carduelis chloris). Ecol Res 22:282–287CrossRefGoogle Scholar
  5. Andersson M (1994) Sexual selection. Princeton University Press, PrincetonGoogle Scholar
  6. Bendich A (1989) Carotenoids and the immune response. J Nutr 119:112–115PubMedGoogle Scholar
  7. Birkhead TR, Fletcher F, Pellat EJ (1998) Sexual selection in the zebra finch Taeniopygia guttata: condition, sex traits and immune capacity. Behav Ecol Sociobiol 44:179–191CrossRefGoogle Scholar
  8. Blount JD, Metcalfe NB, Birkhead TR, Surai PF (2003) Carotenoid modulation of immune function and sexual attractiveness in zebra finch. Science 300:125–127PubMedCrossRefGoogle Scholar
  9. Boa-Amponsem K, Price SHE, Dunnington EA, Siegel PB (2001) Effect of route of inoculation on humoral immune response of White Leghorn chickens selected for high or low antibody response to sheep red blood cells. Poultry Sci 80:1073–1078Google Scholar
  10. Chew BP (1993) Role of carotenoids in the immune response. J Dairy Sci 76:2804–2811PubMedCrossRefGoogle Scholar
  11. Cramp S, Perrins CM (1994) The birds of Western Palaearctic, vol VII. Oxford University Press, OxfordGoogle Scholar
  12. Eley C (1991) Status signalling in the western green finch (Carduelis chloris). Ph.D. thesis, University of Sussex, Brighton, UKGoogle Scholar
  13. Endler JA (1990) On the measurement and classification of colour in studies of animal colour patterns. Biol J Linn Soc 41:315–352Google Scholar
  14. Evans MR, Goldsmith AR, Norris SRA (2000) The effects of testosterone on antibody production and plumage coloration in male house sparrows (Passer domesticus). Behav Ecol Sociobiol 47:156–163CrossRefGoogle Scholar
  15. Faivre B, Gregorie A, Preault M, Cézilly F, Sorci G (2003a) Immune activation rapidly mirrored in a secondary sexual trait. Science 300:103PubMedCrossRefGoogle Scholar
  16. Faivre B, Preault M, Salvadori F, Thery M, Gaillard M, Cézilly F (2003b) Bill colour and immunocompetence in the European blackbird. Anim Behav 65:1125–1131CrossRefGoogle Scholar
  17. Fenoglio S, Cucco M, Malacarne G (2002) The effect of a carotenoid-rich diet on immunocompetence and behavioural performance in moorhen chicks. Ethol Ecol Evol 14:149–156CrossRefGoogle Scholar
  18. Figuerola J, Senar JC, Pascual J (1999) The use of colorimeters on free-living birds: sex, age and locality differences in blue tits (Parus caeruleus) coloration. Ardea 87:269–275Google Scholar
  19. Folstad I, Karter AJ (1992) Parasites, bright males and the immunocompetence handicap. Am Nat 139:603–622CrossRefGoogle Scholar
  20. Gray DA (1996) Carotenoids and sexual dichromatism in North American passerine birds. Am Nat 148:453–480CrossRefGoogle Scholar
  21. Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds: a role for parasites? Science 218:384–387PubMedCrossRefGoogle Scholar
  22. Higgins DA (1996) Comparative immunology of avian species. In: Davison TF, Morris TR, Payne LN (eds) Poultry immunology. Carfax, Abingdon, pp 149–205Google Scholar
  23. Hill GE (1999a) Mate choice, male quality, and carotenoid-based plumage colouration. In: Adams N, Slowtow R (eds) Proceedings of the 22nd International Ornithological Congress. Durban, pp 1654–1668Google Scholar
  24. Hill GE (1999b) Is there an immunological cost to carotenoid-based ornamental coloration? Am Nat 154:589–595PubMedCrossRefGoogle Scholar
  25. Koutsos EA, Calvert CC, Klasing KC (2003) The effects of an acute phase response on tissue carotenoid levels of growing chickens (Gallus gallus domesticus). Comp Biochem Physiol 135A:635–646Google Scholar
  26. Kreukniet MB, van der Zijpp AJ, Nieuwland MGB (1992) Effects of route of immunization, adjuvant and unrelated antigens on the humoral immune response in lines of chickens selected for antibody production against sheep erythrocytes. Vet Immunol Immunopathol 33:115–127PubMedCrossRefGoogle Scholar
  27. Li Z, Nestor KE, Saif YM, Anderson JW (2000) Antibody responses to sheep red blood cell and Brucella abortus antigens in a turkey line selected for increased body weight and its random bred control. Poultry Sci 79:804–809Google Scholar
  28. Lozano GA (1994) Carotenoids, parasites, and sexual selection. Oikos 70:309–311CrossRefGoogle Scholar
  29. Lozano GA (2001) Carotenoids, immunity, and sexual selection: comparing apples and oranges? Am Nat 158:200–203CrossRefPubMedGoogle Scholar
  30. Lynn SE, Houtman AM, Weathers WW, Ketterson ED, Val Nolan JR (2000) Testosterone increases activity but not daily energy expenditure in captive male dark-eyed juncos (Junco hyemalis). Anim Behav 60:581–587PubMedCrossRefGoogle Scholar
  31. Maynard Smith J, Harper DGC (1988) The evolution of aggression: can selection generate variability? Philos Trans R Soc Lond B Biol Sci 319:557–570PubMedCrossRefGoogle Scholar
  32. McGraw KJ, Ardia DR (2003) Carotenoids, immunocompetence, and the information content of sexual colors: an experimental test. Am Nat 162:704–712PubMedCrossRefGoogle Scholar
  33. Møller AP, Petrie M (2002) Condition dependence, multiple sexual signals, and immunocompetence in peacocks. Behav Ecol 13:248–253CrossRefGoogle Scholar
  34. Møller AP, Pomiankowski A (1993) Why have birds got multiple sexual ornaments? Behav Ecol Sociobiol 32:167–176Google Scholar
  35. Møller AP, Christe P, Lux E (1999) Parasitism, host immune function, and sexual selection. Q Rev Biol 74:3–20PubMedCrossRefGoogle Scholar
  36. 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 11:137–159Google Scholar
  37. Munns PL, Lamont SJ (1991) Effects of age and immunization interval on anamnestic response to T-cell-dependent and T-cell-independent antigens in chickens. Poultry Sci 70:2371–2374Google Scholar
  38. Navara KJ, Hill GE (2003) Dietary carotenoid pigments and immune function in a songbird with extensive carotenoid-based plumage coloration. Behav Ecol 14:909–916CrossRefGoogle Scholar
  39. Olson VA, Owens IPF (1998) Costly sexual signals: are carotenoids rare, risky or required. Trends Ecol Evol 13:510–514CrossRefGoogle Scholar
  40. Saks L, McGraw K, Hõrak P (2003a) How feather colour reflects its carotenoid content. Funct Ecol 17:555–561CrossRefGoogle Scholar
  41. Saks L, Ots I, Hõrak P (2003b) Carotenoid-based plumage coloration of male greenfinches reflects health and immunocompetence. Oecologia 134:301–307PubMedGoogle Scholar
  42. Senar JC, Polo V, Uribe F, Camerino M (2000) Status signalling, metabolic rate and body mass in the siskin: the costs of being subordinate. Anim Behav 59:103–110PubMedCrossRefGoogle Scholar
  43. Stradi R, Celentano G, Rossi E, Rovati G, Pastore M (1995) Carotenoids in bird plumage. I. The carotenoid pattern in a series of Palearctic Carduelinae. Comp Biochem Physiol 110B:131–143Google Scholar
  44. Tella JL, Negro JJ, Rodríguez-Estrella R, Blanco G, Forero MG, Blázquez MC, Hiraldo F (1998) A comparison of spectrophotometry and color charts for evaluating total plasma carotenoids in wild birds. Physiol Zool 71:708–711PubMedGoogle Scholar
  45. 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 266:1–12CrossRefGoogle Scholar
  46. Wedekind C (1992) Detailed information about parasites revealed by sexual ornamentation. Proc R Soc Lond B Biol Sci 247:169–174CrossRefGoogle Scholar
  47. Wedekind C, Folstad I (1994) Adaptive or nonadaptive immunosuppression by sex hormones? Am Nat 143:936–938CrossRefGoogle Scholar
  48. Wegmann TG, Smithies O (1966) A simple hemagglutination system requiring small amounts of red cells and antibodies. Transfusion 6:67–73CrossRefGoogle Scholar
  49. Westneat DF, Birkhead TR (1998) Alternative hypotheses linking the immune system and mate choice for good genes. Proc R Soc Lond B Biol Sci 265:1065–1073CrossRefGoogle Scholar
  50. Wingfield JC, Hegner RE, Dufty AM, Ball GF (1990) The “challenge hypothesis”—theoretical implications for patterns of testosterone secretion, mating systems and breeding strategies. Am Nat 136:829–846CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  1. 1.Department of Evolutionary BiologyEstación Biológica de Doñana, CSICSevilleSpain

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