Skip to main content
Log in

Parental effects on carotenoid-based plumage coloration in nestling great tits, Parus major

  • Original Article
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

Carotenoid pigments have attracted much interest in behavioural and evolutionary ecology because of their dual function in immune physiology and as color signals. In vertebrates, carotenoids must ultimately be obtained from the diet, and the mechanisms and magnitude of this environmental dependence are central for understanding carotenoid signal functions and evolution. In the present cross-fostering experiment with great tits Parus major, we investigate pre- and postnatal parental effects (egg yolk carotenoids, parental coloration) on nestling size and carotenoid coloration, using HPLC analysis of egg yolk carotenoids, and a reflectance-based measure of ‘chroma’ that reflects the plumage pigment concentration. Both rearing environment and origin influenced offspring size and plumage chroma. Maternal allocation of carotenoids to eggs had a weak positive effect on nestling plumage chroma, whereas we found no prenatal maternal effects (egg size or yolk carotenoid concentration) on size. Nestling plumage chroma was also significantly predicted by the chroma of the rearing father, but not by the color of the rearing mother or either of the original (genetical) parents. Thus, both prenatal maternal effects and postnatal paternal effects influence the carotenoid-based plumage coloration of nestling great tits. Future studies will reveal if parental effects have long-term consequences for plumage development and associated fitness components.

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

Similar content being viewed by others

References

  • Andersson S, Pryke SR, Örnborg J, Lawes MJ, Andersson M (2002) Multiple receivers, multiple ornaments, and a trade-off between agonistic and epigamic signaling in a widowbird. Am Nat 160:683–691

    Article  PubMed  Google Scholar 

  • Andersson S, Uller T, Löhmus M, Sundström F (2004) Effects of egg yolk testosterone on growth and immunity in a precocial bird. J Evol Biol 17:501–505

    Article  PubMed  CAS  Google Scholar 

  • Andersson S, Prager M (2006) Quantifying colors. In: Hill GE, McGraw KJ (eds) Bird coloration, Vol 1. Mechanisms and measurements. Harvard Univ. Press, Cambridge, MA (USA), pp 41–89

    Google Scholar 

  • Bendich A (1989) Carotenoids and the immune response. J Nutr 119:112–115

    PubMed  CAS  Google Scholar 

  • Blount JD, Houston DC, Møller AP (2000) Why egg yolk is yellow. Trends Ecol Evol 15:47–49

    Article  PubMed  Google Scholar 

  • Boileau TWM, Moore AC, Erdman JW (1999) Carotenoids and vitamin A. In: Papas AM (eds) Antioxidant status, diet, nutrition, and health. CRC, New York, pp 133–157

    Google Scholar 

  • Bortolotti GR, Tella JL, Forero MG, Dawson RD, Negro JJ (2000) Genetics, local environment and health as factors influencing plasma carotenoids in wild American kestrels (Falco sparverius). Proc R Soc Lond B 267:1433–1438

    Article  CAS  Google Scholar 

  • Brush AH (1990) Metabolism of carotenoid pigments in birds. FASEB J 4:2969–2977

    PubMed  CAS  Google Scholar 

  • Burley N (1988) The differential-allocation hypothesis. Am Nat 132:611–628

    Article  Google Scholar 

  • Cramp S, Perrins CM (1993) The birds of the western Palearctic, vol 8. Oxford University, Oxford

    Google Scholar 

  • Dufva R, Allander K (1995) Intraspecific variation in plumage coloration reflects immune-response in Great Tit (Parus major) Males. Funct Ecol 9:785–789

    Article  Google Scholar 

  • Eeva T, Lehikoinen E, Ronka M (1998) Air pollution fades the plumage of the Great Tit. Funct Ecol 12:607–612

    Article  Google Scholar 

  • Fitze PS, Kölliker M, Richner H (2003a) Effects of common origin and common environment on nestling plumage coloration in the great tit (Parus major). Evolution 57:144–150

    PubMed  Google Scholar 

  • Fitze PS, Tschirren B, Richner H (2003b) Carotenoid-based colour expression is determined early in nestling life. Oecologia 137:148–152

    Article  PubMed  Google Scholar 

  • Goodwin TW (1986) Metabolism, nutrition, and function of carotenoids. Annu Rev Nutr 6:274–297

    Article  Google Scholar 

  • Haq AU, Bailey CA, Chinnah A (1996) Effect of beta-carotene, canthaxanthin, lutein, and vitamin E on neonatal immunity of chicks when supplemented in the broiler breeder diets. Poult Sci 75:1092–1097

    PubMed  CAS  Google Scholar 

  • Hill GE, Inouye CY, Montgomerie R (2002) Dietary carotenoids predict plumage coloration in wild house finches. Proc R Soc Lond B 269:1119–1124

    Article  CAS  Google Scholar 

  • Hõrak P, Vellau H, Ots I, Møller AP (2000) Growth conditions affect carotenoid-based plumage coloration of great tit nestlings. Naturwissenschaften 87:460-464

    Article  PubMed  Google Scholar 

  • Hõrak P, Ots I, Vellau H, Spottiswoode C, Møller AP (2001) Carotenoid-based plumage coloration reflects hemoparasite infection and local survival in breeding great tits. Oecologia 126:166–173

    Article  Google Scholar 

  • Johnsen A, Delhey K, Andersson SA, Kempenaers B (2003) Plumage colour in nestling blue tits: sexual dichromatism, condition dependence and genetic effects. Proc R Soc Lond B 270:1263–1270

    Article  Google Scholar 

  • Kilner R (1997) Mouth colour is a reliable signal of need in begging canary nestlings. Proc R Soc Lond Ser B 264:963–968

    Article  Google Scholar 

  • Kirkpatrick M, Lande R (1989) The evolution of maternal characters. Evolution 43:485–503

    Article  Google Scholar 

  • Kluijver HN (1950) Daily routines of the great tit, Parus m. major L. Ardea 38:99–135

    Google Scholar 

  • Kowalczyk K, Daiss J, Halpern J, Roth TF (1985) Quantification of maternal-fetal IgG transport to the chicken. Immunology 54:755–762

    PubMed  CAS  Google Scholar 

  • Krebs EA, Putland DA (2004) Chic chicks: the evolution of chick ornamentation in rails. Behav Ecol 15:946–951

    Article  Google Scholar 

  • Krinsky NI (2001) Carotenoids as antioxidants. Nutrition 17:815–817

    Article  PubMed  CAS  Google Scholar 

  • Limbourg T, Mateman AC, Andersson S, Lessells CM (2004) Female blue tits adjust parental effort to manipulated male UV attractiveness. Proc R Soc Lond B 271:1903–1908

    Article  Google Scholar 

  • Linville SU, Breitwisch R, Schilling AJ (1998) Plumage brightness as an indicator of parental care in northern cardinals. Anim Behav 55:119–127

    Article  PubMed  Google Scholar 

  • Littel RC, Milliken GA, Stroup WW, Wolfinger RD (2000) SAS system for mixed models. SAS Institute, Cary, North Carolina

    Google Scholar 

  • Lyon BE, Eadie JM, Hamilton LD (1994) Parental choice selects for ornamental plumage in coot chicks. Nature 371:240–243

    Article  Google Scholar 

  • McGraw KJ, Hill GE (2000) Differential effects of endoparasitism on the expression of carotenoid- and melanin-based ornamental coloration. Proc R Soc Lond B 267:1525–1531

    Article  CAS  Google Scholar 

  • McGraw KJ, Beebee MD, Hill GE, Parker RS (2003) Lutein-based plumage coloration in songbirds is a consequence of selective pigment incorporation into feathers. Comp Biochem Physiol 135B:689–696

    CAS  Google Scholar 

  • McGraw KJ, Adkins-Regan E, Parker RS (2005) Maternally derived carotenoid pigments affect offspring survival, sex ratio, and sexual attractiveness in a colourful songbird. Naturwissenschaften 92:375–380

    Article  PubMed  CAS  Google Scholar 

  • Mousseau TA, Fox CW (1998) The adaptive significance of maternal effects. Trends Ecol Evol 13:403–407

    Article  Google Scholar 

  • Nys Y (2000) Dietary carotenoids and egg yolk coloration—a review. Arch Geflugelkunde 64:45–54

    CAS  Google Scholar 

  • Partali V, Liaaenjensen S, Slagsvold T, Lifjeld JT (1987) Carotenoids in food-chain studies. 2. The food-chain of Parus spp. monitored by carotenoid analysis. Comp Biochem Physiol 87B:885–888

    CAS  Google Scholar 

  • Pryke SR, Andersson S (2005) Experimental evidence for female choice and energetic costs of male tail elongation in red-collared widowbirds. Biol J Linn Soc 86:35–43

    Article  Google Scholar 

  • Quinn G, Keough M (2002) Experimental design and data analysis for biologists. Cambridge University, Cambridge

    Google Scholar 

  • Saino N, Ninni P, Calza S, Martinelli R, De Bernardi F, Møller AP (2000) Better red than dead: carotenoid-based mouth coloration reveals infection in barn swallow nestlings. Proc R Soc Lond B 267:57–61

    Article  CAS  Google Scholar 

  • Saino N, Bertacche V, Ferrari RP, Martinelli R, Møller AP, Stradi R (2002) Carotenoid concentration in barn swallow eggs is influenced by laying order, maternal infection and paternal ornamentation. Proc R Soc Lond B 269:1729–1733

    Article  CAS  Google Scholar 

  • Saino N, Ferrari R, Romano M, Martinelli R, Møller AP (2003) Experimental manipulation of egg carotenoids affects immunity of barn swallow nestlings. Proc R Soc Lond B 270:2485–2489

    Article  Google Scholar 

  • Saks L, McGraw K, Hõrak P (2003) How feather colour reflects its carotenoid content. Funct Ecol 17:555–561

    Article  Google Scholar 

  • Schwabl H (1993) Yolk is a source of maternal testosterone for developing birds. Proc Natl Acad Sci USA 90:11446–11450

    Article  PubMed  CAS  Google Scholar 

  • Schwabl H (1996) Environment modifies the testosterone levels of a female bird and its eggs. J Exp Zool 276:157–163

    Article  PubMed  CAS  Google Scholar 

  • Senar JC, Figuerola J, Pascual J (2002) Brighter yellow blue tits make better parents. Proc R Soc Lond B 269:257–261

    Article  CAS  Google Scholar 

  • Sheldon BC (2000) Differential allocation: tests, mechanisms and implications. Trends Ecol Evol 15:397–402

    Article  PubMed  Google Scholar 

  • Slagsvold T, Lifjeld JT (1985) Variation in plumage coloration of the great tit Parus major in relation to habitat, season, and food. J Zool Lond 206A:321–328

    Google Scholar 

  • Snijders TAB, Bosker RJ (1999) Multilevel analysis. An introduction to basic and advanced multilevel modeling. SAGE, London, pp 102

    Google Scholar 

  • Stradi R (1998) The colour of flight: carotenoids in bird plumage. Gruppo editoriale informatico, Milan

    Google Scholar 

  • Surai PF, Speake BK (1998) Distribution of carotenoids from the yolk to the tissues of the chick embryo. J Nutr Biochem 9:645–651

    Article  CAS  Google Scholar 

  • Surai PF, Ionov IA, Kuchmistova EF, Noble RC, Speake BK (1998) The relationship between the levels of alpha-tocopherol and carotenoids in the maternal feed, yolk and neonatal tissues: comparison between the chicken, turkey, duck and goose. J Sci Food Agric 76:593–598

    Article  CAS  Google Scholar 

  • Surai P (2002) Natural antioxidants in avian nutrition and reproduction. Nottingham University Press, Nottingham, pp 129–200

    Google Scholar 

  • Thompson CW, Hillgarth N, Leu M, McClure HE (1997) High parasite load in house finches (Carpodacus mexicanus) is correlated with reduced expression of a sexually selected trait. Am Nat 149:270–294

    Article  Google Scholar 

  • Tschirren B, Fitze PS, Richner H (2003) Proximate mechanisms of variation in the carotenoid-based plumage coloration of nestling great tits (Parus major L.). J Evol Biol 16:91–100

    Article  PubMed  CAS  Google Scholar 

  • Tschirren B, Fitze PS, Richner H (2005) Carotenoid-based nestling colouration and parental favouritism in the great tit. Oecologia 143:477–482

    Article  PubMed  Google Scholar 

  • von Schantz TS, 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

    Article  Google Scholar 

  • West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University, New York

    Google Scholar 

  • Wolf JB, Brodie ED III, Cheverud JM, Moore AJ, Wade MJ (1998) Evolutionary consequences of indirect genetic effects. Trends Ecol Evol 13:64–69

    Article  Google Scholar 

Download references

Acknowledgements

We thank Mats Hulander, Nina Jansson, and Uno Unger for assistance in the field and Maria von Post for help in the laboratory. Three anonymous reviewers provided valuable comments on a previous draft of this paper. Roche Vitamins, (Basel, Switzerland) generously provided us with all carotenoid standards. The work was supported by Lars Hiertas Minne (to C. I.), Wenner-Gren Foundations (to T. U.) and The Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning (to S. A.). The study was conducted in full compliance with Swedish laws and regulation, including ethical permit from Centrala Försökdjursnämnden, CFN.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Caroline Isaksson.

Additional information

Communicated by K. McGraw

Rights and permissions

Reprints and permissions

About this article

Cite this article

Isaksson, C., Uller, T. & Andersson, S. Parental effects on carotenoid-based plumage coloration in nestling great tits, Parus major . Behav Ecol Sociobiol 60, 556–562 (2006). https://doi.org/10.1007/s00265-006-0200-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-006-0200-6

Keywords

Navigation