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What is the value of a yellow patch? Assessing the signalling role of yellow colouration in the European serin

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Abstract

Sexual selection promotes the evolution of signals, many of which can reliably indicate condition, health or good genes of individuals. In order to be evolutionarily stable, indicator signals must be costly to produce. Carotenoid colouration evolved in many species by sexual selection. Carotenoids besides acting as pigments have been implicated in immune defence and antioxidation which makes them likely candidates for honest signalling. A trade-off for carotenoid availability was proposed as the basis for signal honesty. Alternatively, it was suggested that carotenoid colouration is not advertising the presence of the pigment per se, but the quality of antioxidant resources which then affect carotenoid concentration. One possibility is that carotenoid-based colouration could signal colourless antioxidant mechanisms, which are partially regulated by vitamins. β-Carotene is one of the most common precursors of vitamin A and, although present in bird diet, is not available for feather colouration. If an indirect association exists between carotenoid signal and condition, then manipulation of β-carotene concentration could reveal that this link is indirect. We tested this by conditioning the availability of β-carotene in the diet of a cardueline finch with yellow carotenoid colouration during moult. β-Carotene-supplemented males had higher plasma carotenoid concentration and higher response to a cellular immunity challenge (phytohaemagglutinin (PHA)) than control males. β-Carotene-supplemented males also had more saturated plumage colouration and were preferred by females in a mate choice test. Our results support the possibility of an indirect role for yellow carotenoid colouration.

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References

  • Aguilera E, Amat J (2007) Carotenoids, immune response and the expression of sexual ornaments in male greenfinches (Carduelis chloris). Naturwissenschaften 94:895–902

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • Baeta R, Faivre B, Motreuil S, Gaillard M, Moreau J (2008) Carotenoid trade-off between parasitic resistance and sexual display: an experimental study in the blackbird (Turdus merula). Proc R Soc Lond B 275:427–434

    Article  CAS  Google Scholar 

  • Behnke JM, McGregor PK, Shepherd M, Wiles R, Barnard C, Gilbert FS, Hurst JL (1995) Identity, prevalence and intensity of infestation with wing feather mites on birds (Passeriformes) from the Setubal Peninsula of Portugal. Exp Appl Acarol 19:443–458

    Google Scholar 

  • Behnke J, McGregor P, Cameron J, Hartley I, Shepherd M, Gilbert F, Barnard C, Hurst J, Gray S, Wiles R (1999) Semi-quantitative assessment of wing feather mite (Acarina) infestations on passerine birds from Portugal. Evaluation of the criteria for accurate quantification of mite burdens. J Zool 248:337–347

    Article  Google Scholar 

  • Bendich A (1989) Symposium conclusions: biological actions of carotenoids. J Nutr 119:135–136

    CAS  PubMed  Google Scholar 

  • Bendich A, Olson JA (1989) Biological actions of carotenoids. FASEB J 3:1927–1932

    CAS  PubMed  Google Scholar 

  • Bertrand S, Alonso-Alvarez C, Devevey G, Faivre B, Prost J, Sorci G (2006a) Carotenoids modulate the trade-off between egg production and resistance to oxidative stress in zebra finches. Oecologia 147:576–584

    Article  PubMed  Google Scholar 

  • Bertrand S, Faivre B, Sorci G (2006b) Do carotenoid-based sexual traits signal the availability of non-pigmentary antioxidants? J Exp Biol 209:4414–4419

    Article  CAS  PubMed  Google Scholar 

  • Biard C, Surai PF, Møller AP (2006) Carotenoid availability in diet and phenotype of blue and great tit nestlings. J Exp Biol 209:1004–1015

    Article  CAS  PubMed  Google Scholar 

  • Biesalski HK, Chichili GR, Frank J, von Lintig J, Nohr D (2007) Conversion of β-carotene to retinal pigment. In: Gerald L (ed) Vitamins & hormones, vol 75. Academic Press, San Diego, USA, p 117–130

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Blount JD (2004) Carotenoids and life-history evolution in animals. Arch Biochem Biophys 430:10–15

    Article  CAS  PubMed  Google Scholar 

  • Blount JD, Surai PF, Houston DC, Møller AP (2001) The relationship between dietary and yolk carotenoid composition in a wild bird: a supplemental feeding study of lesser black-backed gulls (Larus fuscus). Br Poult Sci 42:S84–S85

    Google Scholar 

  • Blount JD, Metcalfe NB, Arnold KE, Surai PF, Devevey GL, Monaghan P (2003) Neonatal nutrition, adult antioxidant defences and sexual attractiveness in the zebra finch. Proc R Soc Lond B 270:1691–1696

    Article  CAS  Google Scholar 

  • Bruzzone OA, Corley JC (2011) Which is the best experimental design in animal choice tests? Anim Behav 82:161–169

    Article  Google Scholar 

  • Chew BP (1993) Role of carotenoids in the immune response. J Dairy Sci 76:2804–2811

    Article  CAS  PubMed  Google Scholar 

  • Chew BP, Park JS (2004) Carotenoid action on the immune response. J Nutr 134:257S–261S

    CAS  PubMed  Google Scholar 

  • Costantini D, Møller AP (2008) Carotenoids are minor antioxidants for birds. Funct Ecol 22:367–370

    Article  Google Scholar 

  • Cramp S, Perrins CM (eds) (1994) Handbook of the birds of Europe, the Middle East and North Africa—the birds of the Western Palearctic, vol VIII—crows to finches. Oxford University Press, Oxford

    Google Scholar 

  • Cucco M, Guasco B, Malacarne G, Ottonelli R (2006) Effects of β-carotene supplementation on chick growth, immune status and behaviour in the grey partridge, Perdix perdix. Behav Process 73:325–332

    Article  CAS  Google Scholar 

  • D’Ambrosio DN, Clugston RD, Blaner WS (2011) Vitamin A metabolism: an update. Nutrients 3:63–103

    Article  PubMed Central  PubMed  Google Scholar 

  • Debier C, Larondelle Y (2005) Vitamins A and E: metabolism, roles and transfer to offspring. Br J Nutr 93:153–174

    Article  CAS  PubMed  Google Scholar 

  • del Val E, Senar J, Garrido-Fernández J, Jarén M, Borràs A, Cabrera J, Negro J (2009) The liver but not the skin is the site for conversion of a red carotenoid in a passerine bird. Naturwissenschaften 96:797–801

    Article  CAS  PubMed  Google Scholar 

  • El-Agamey A, Lowe GM, McGarvey DJ, Mortensen A, Phillip DM, Truscott TG, Young AJ (2004) Carotenoid radical chemistry and antioxidant/pro-oxidant properties. Arch Biochem Biophys 430:37–48

    Article  CAS  PubMed  Google Scholar 

  • Endler J (1983) Natural and sexual selection on color patterns in poeciliid fishes. Environ Biol Fish 9:173–190

    Article  Google Scholar 

  • Evans JP, Kelley JL, Bisazza A, Finazzo E, Pilastro A (2004) Sire attractiveness influences offspring performance in guppies. Proc R Soc Lond B 271:2035–2042

    Article  Google Scholar 

  • Evans SR, Hinks AE, Wilkin TA, Sheldon BC (2010) Age, sex and beauty: methodological dependence of age- and sex-dichromatism in the great tit Parus major. Biol J Linn Soc 101:777–796

    Article  Google Scholar 

  • Faivre B, Préault M, Salvadori F, Théry M, Gaillard M, Cézilly F (2003) Bill colour and immunocompetence in the European blackbird. Anim Behav 65:1125–1131

    Article  Google Scholar 

  • Fenoglio S, Cucco M, Malacarne G (2002) The effect of a carotenoid-rich diet on immunocompetence and behavioural performances in Moorhen chicks. Ethol Ecol Evol 14:149–156

    Article  Google Scholar 

  • Figuerola J, Senar JC (2007) Serins with intermediate brightness have a higher survival in the wild. Oikos 116:636–641

    Article  Google Scholar 

  • Figuerola J, Domenech J, Senar JC (2003) Plumage colour is related to ectosymbiont load during moult in the serin, Serinus serinus: an experimental study. Anim Behav 65:551–557

    Article  Google Scholar 

  • Galluzzi L, Kepp O, Trojel-Hansen C, Kroemer G (2012) Mitochondrial control of cellular life, stress, and death. Circ Res 111:1198–1207

    Article  CAS  PubMed  Google Scholar 

  • Goodwin TW (1984) The biochemistry of carotenoids, vol II, animals. Chapman & Hall, New York

    Book  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Hart N, Partridge J, Cuthill I, Bennett A (2000) Visual pigments, oil droplets, ocular media and cone photoreceptor distribution in two species of passerine bird: the blue tit (Parus caeruleus L.) and the blackbird (Turdus merula L.). J Comp Physiol A 186:375–387

    Article  CAS  PubMed  Google Scholar 

  • Hartley RC, Kennedy MW (2004) Are carotenoids a red herring in sexual display? Trends Ecol Evol 19:353–354

    Article  PubMed  Google Scholar 

  • Hasselquist D, Nilsson J-Å (2012) Physiological mechanisms mediating costs of immune responses: what can we learn from studies of birds? Anim Behav 83:1303–1312

    Article  Google Scholar 

  • Håstad O, Victorsson J, Ödeen A (2005) Differences in color vision make passerines less conspicuous in the eyes of their predators. Proc Natl Acad Sci U S A 102:6391–6394

    Article  PubMed Central  PubMed  Google Scholar 

  • Hill GE (1990) Female house finches prefer colourful males: sexual selection for a condition-dependent trait. Anim Behav 40:563–572

    Article  Google Scholar 

  • Hill GE (1994) Geographic variation in male ornamentation and female mate preference in the House finch—a comparative test of models of sexual selection. Behav Ecol 5:64–73

    Article  Google Scholar 

  • Hill GE (1999) Is there an immunological cost to carotenoid-based ornamental coloration? Am Nat 154:589–595

    Article  PubMed  Google Scholar 

  • Hill GE (2006) Female mate choice for ornamental coloration. In: Hill GE, McGraw K (eds) Bird coloration: function and evolution, vol II. Harvard University Press, London, pp 137–200

    Google Scholar 

  • Hill GE, Johnson JD (2012) The vitamin A–redox hypothesis: a biochemical basis for honest signaling via carotenoid pigmentation. Am Nat 180:E127–E150

    Article  PubMed  Google Scholar 

  • Hõrak P, Saks L (2003) Animal allure and health linked by plant pigments. BioEssays 25:746–747

    Article  PubMed  Google Scholar 

  • Huggins K, Navara K, Mendonça M, Hill G (2010) Detrimental effects of carotenoid pigments: the dark side of bright coloration. Naturwissenschaften 97:637–644

    Article  CAS  PubMed  Google Scholar 

  • Jakob E, Marshall S, Uetz G (1996) Estimating fitness: a comparison of body condition indices. Oikos 77:61–67

    Article  Google Scholar 

  • Johnson K, Rosetta D, Burley DN (1993) Preferences of female American goldfinches (Carduelis tristis) for natural and artificial male traits. Behav Ecol 4:138–143

    Article  Google Scholar 

  • Kopena R, López P, Martín J (2014) Relative contribution of dietary carotenoids and vitamin E to visual and chemical sexual signals of male Iberian green lizards: an experimental test. Behav Ecol Sociobiol 68:571–581

    Article  Google Scholar 

  • Krinsky NI (1989) Antioxidant functions of carotenoids. Free Radic Biol Med 7:617–635

    Article  CAS  PubMed  Google Scholar 

  • Leitão AV, Monteiro AH, Mota PG (2014) Ultraviolet reflectance influences female preference for colourful males in the European serin. Behav Ecol Sociobiol 68:63–72

    Article  Google Scholar 

  • Lozano GA (1994) Carotenoids, parasites, and sexual selection. Oikos 70:309–311

    Article  Google Scholar 

  • Maia R, Eliason CM, Bitton PP, Doucet SM, Shawkey MD (2013) pavo: an R package for the analysis, visualization and organization of spectral data. Methods Ecol Evol 4:906–913

    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 

  • Martínez A, Rodríguez-Gironés MA, As B, Costas M (2008) Donator acceptor map for carotenoids, melatonin and vitamins. J Phys Chem A 112:9037–9042

    Article  PubMed  Google Scholar 

  • McGraw K (2006) Mechanics of carotenoid-based coloration. In: Hill GE, McGraw K (eds) Bird coloration: mechanisms and measurements, vol I. Harvard University Press, London, pp 177–242

    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 

  • McGraw KJ, Ardia DR (2005) Sex differences in carotenoid status and immune performance in zebra finches. Evol Ecol Res 7:251–262

    Google Scholar 

  • McGraw KJ, Hill GE, Stradi R, Parker RS (2001) The influence of carotenoid acquisition and utilization on the maintenance of species-typical plumage pigmentation in male American goldfinches (Carduelis tristis) and Northern Cardinals (Cardinalis cardinalis). Physiol Biochem Zool 74:843–852

    Article  CAS  PubMed  Google Scholar 

  • McGraw KJ, Hill GE, Parker RS (2005) The physiological costs of being colourful: nutritional control of carotenoid utilization in the American goldfinch, Carduelis tristis. Anim Behav 69:653–660

    Article  Google Scholar 

  • McWhinney SLL, Bailey CA (1989) Immunoenhancing effect of β-carotene in chicks. Poult Sci 68(suppl 1):94 (Abstr.)

    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 

  • Mougeot F (2008) Ornamental comb colour predicts T-cell-mediated immunity in male red grouse Lagopus lagopus scoticus. Naturwissenschaften 95:125–132

    Article  CAS  PubMed  Google Scholar 

  • Navara KJ, Hill GE (2003) Dietary carotenoid pigments and immune function in a songbird with extensive carotenoid-based plumage coloration. Behav Ecol 14:909–916

    Article  Google Scholar 

  • Navarro C, Pérez-Contreras T, Avilés J, McGraw K, Soler J (2010) Beak colour reflects circulating carotenoid and vitamin A levels in spotless starlings (Sturnus unicolor). Behav Ecol Sociobiol 64:1057–1067

    Article  Google Scholar 

  • Ninni P, Fd L, Saino N, Haussy C, Møller AP (2004) Antioxidants and condition-dependence of arrival date in a migratory passerine. Oikos 105:55–64

    Article  Google Scholar 

  • Nolan PM, Hill GE (2004) Female choice for song characteristics in the house finch. Anim Behav 67:403–410

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Osorio D, Miklósi A, Gonda Z (1999) Visual ecology and perception of coloration patterns by domestic chicks. Evol Ecol 13:673–689

    Article  Google Scholar 

  • Ots I, Murumägi A, Hõrak P (1998) Haematological health state indices of reproducing great tits: methodology and sources of natural variation. Funct Ecol 12:700–707

    Article  Google Scholar 

  • Ots I, Kerimov AB, Ivankina EV, Ilyina TA, Hõrak P (2001) Immune challenge affects basal metabolic activity in wintering great tits. Proc R Soc Lond B 268:1175–1181

    Article  CAS  Google Scholar 

  • Pagani-Nuñez E, Senar JC (2012) Changes in carotenoid-based plumage colour in relation to age in European Serins Serinus serinus. Ibis 154:155–160

    Article  Google Scholar 

  • Pérez-Rodriguez L, Mougeot F, Alonso-Alvarez C, Blas J, Vinuela J, Bortolotti GR (2008) Cell-mediated immune activation rapidly decreases plasma carotenoids but does not affect oxidative stress in red-legged partridges (Alectoris rufa). J Exp Biol 211:2155–2161

    Article  PubMed  Google Scholar 

  • Pérez-Rodriguez L, Mougeot F, Alonso-Alvarez C (2010) Carotenoid-based coloration predicts resistance to oxidative damage during immune challenge. J Exp Biol 213:1685–1690

    Article  PubMed  Google Scholar 

  • Peters A, Delhey K, Denk AG, Kempenaers B (2004) Trade-offs between immune investment and sexual signaling in male mallards. Am Nat 164:51–59

    Article  PubMed  Google Scholar 

  • Peters A, Magdeburg S, Delhey K (2011) The carotenoid conundrum: improved nutrition boosts plasma carotenoid levels but not immune benefits of carotenoid supplementation. Oecologia 166:35–43

    Article  PubMed  Google Scholar 

  • Pike TW, Blount JD, Lindström J, Metcalfe NB (2007) Availability of non-carotenoid antioxidants affects the expression of a carotenoid-based sexual ornament. Biol Lett 3:353–356

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • R Development Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, http://www.R-project.org

  • 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, Ots I, Hõrak P (2003) Carotenoid-based plumage coloration of male greenfinches reflects health and immunocompetence. Oecologia 134:301–307

    Article  PubMed  Google Scholar 

  • Schulte-Hostedde AI, Zinner B, Millar JS, Hickling GJ (2005) Restitution of mass-size residuals: validating body condition indices. Ecology 86:155–163

    Article  Google Scholar 

  • Searcy WA, Nowicki S (2005) The evolution of animal communication: reliability and deception in signaling systems. Princeton University Press, Princeton

    Google Scholar 

  • Simons MJP, Verhulst S (2011) Zebra finch females prefer males with redder bills independent of song rate—a meta-analysis. Behav Ecol 22:755–762

    Article  Google Scholar 

  • Simons MJP, Cohen AA, Verhulst S (2012) What does carotenoid-dependent coloration tell? Plasma carotenoid level signals immunocompetence and oxidative stress state in birds—a meta-analysis. PLoS One 7:e43088

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Stillwell W, Nahmias S (1983) Effect of retinol and retinoic acid on P/O ratios of coupled mitochondria. Biochem Int 6:385–392

    CAS  PubMed  Google Scholar 

  • Stradi R, Celentano G, Nava D (1995a) Separation and identification of carotenoids in bird’s plumage by high-performance liquid chromatography-diode-array detection. J Chromatogr B 670:337–348

    Article  CAS  Google Scholar 

  • Stradi R, Celentano G, Rossi E, Rovati G, Pastore M (1995b) Carotenoids in bird plumage-I. The carotenoid pattern in a series of Palearctic Carduelinae. Comp Biochem Physiol B 110:131–143

    Article  Google Scholar 

  • Sundberg J (1995) Female yellowhammers (Emberiza citrinella) prefer yellower males: a laboratory experiment. Behav Ecol Sociobiol 37:275–282

    Article  Google Scholar 

  • Surai AP (2002) Natural antioxidants in avian nutrition and reproduction. Nottingham University Press, Nottingham

    Google Scholar 

  • Tella JL, Lemus JA, Carrete M, Blanco G (2008) The PHA test reflects acquired T-cell mediated immunocompetence in birds. PLoS One 3:e3295

    Article  PubMed Central  PubMed  Google Scholar 

  • Toomey M, McGraw K (2012) Mate choice for a male carotenoid-based ornament is linked to female dietary carotenoid intake and accumulation. BMC Evol Biol 12:3

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • von Lintig J (2010) Colors with functions: elucidating the biochemical and molecular basis of carotenoid metabolism. Annu Rev Nutr 30:35–56

    Article  Google Scholar 

  • Vorobyev M, Osorio D, Bennett A, Marshall N, Cuthill I (1998) Tetrachromacy, oil droplets and bird plumage colours. J Comp Physiol A 183:621–633

    Article  CAS  PubMed  Google Scholar 

  • West AP, Shadel GS, Ghosh S (2011) Mitochondria in innate immune responses. Nat Rev Immunol 11:389–402

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We are grateful to Marta Costa for her field assistance, to Licínio Manco for lab help and to Antónia Conceição, from ESAC, for the supply of sheep blood. We also thank Jim Johnson and two anonymous reviewers for useful comments. This work was supported by a research grant (PTDC/BIA-BEC/105325/2008) to PGM and a PhD fellowship (SFRH/BD/44837/2008) to ST, both by Fundação para a Ciência e a Tecnologia.

Ethical standards

All experiments were performed in accordance to Portuguese legislation for research on animal behaviour and were conducted under license permits: 258/2009/CAPT to PGM and 259/2009/CAPT to ST, by Instituto da Conservação da Natureza e da Biodiversidade (ICNB).

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  1. Department of Life Sciences, University of Coimbra, Apt. 3046, 3301-401, Coimbra, Portugal

    Sandra Trigo & Paulo G. Mota

  2. CIBIO, Research Center in Biodiversity and Genetic Resources, University of Porto, Campus Agrário de Vairão, 4485-661, Vairão, Portugal

    Sandra Trigo & Paulo G. Mota

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Trigo, S., Mota, P.G. What is the value of a yellow patch? Assessing the signalling role of yellow colouration in the European serin. Behav Ecol Sociobiol 69, 481–490 (2015). https://doi.org/10.1007/s00265-014-1860-2

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