Dietary flavonoids enhance conspicuousness of a melanin-based trait in male blackcaps but not of the female homologous trait or of sexually monochromatic traits

Journal of Evolutionary Biology

Volumn 22, Issue 8, 2009, Pages 1649-1657

  Catoni, C ^a,b   Peters, A ^b   Schaefer, H M ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b MAX PLANCK INSTITUTE FOR ORNITHOLOGY   (Germany)

Author keywords

Antioxidants; Bird; Carotenoids; Immune competence; Mechanisms; Melanin; Plumage colouration; Sexual selection; Signal; Signal honesty

Indexed keywords

FLAVONOID; MELANIN;

ANTIOXIDANT; GENOTYPE; HONEST SIGNALING; IMMUNE RESPONSE; LIFE HISTORY TRAIT; MELANIN; PASSERINE; PHENOTYPE; SEXUAL SELECTION; SIGNALING;

ANIMAL; ARTICLE; COLOR; DIET; FEATHER; MALE; METABOLISM; PHENOTYPE; PHYSIOLOGY; SONGBIRD;

ANIMALS; COLOR; DIET; FEATHERS; FLAVONOIDS; MALE; MELANINS; PHENOTYPE; SONGBIRDS;

ANIMALIA; AVES; SYLVIA ATRICAPILLA;

EID: 67650465540     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/j.1420-9101.2009.01778.x     Document Type: Article

References (70)

1. Andersson, S. 2000. Efficacy and content in avian colour signals. In : Animal Signals: Signaling and Signal Design in Animal Communication (Y. Epsmark, T. Amundsen G. Rosenqvist, eds pp. 47 60. Tapir, Trondheim.
2. Arck, P.C., Overall, R., Spatz, K., Liezman, C., Handjiski, B., Klapp, B.F., Birch-Machin, M.A. Peters, E.M.J. 2006. Towards a "free radical theory of graying": melanocyte apoptosis in the aging human hair follicle is an indicator of oxidative stress induced tissue damage. FASEB J. 20 : 1567 1569.
3. Beecher, G.R. 2003. Overview of dietary flavonoids: nomenclature, occurrence and intake. J. Nutr. 133 : 3248 3253.
4. Benjamini, Y. Hochberg, Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. 57 : 289 300.
5. Berthold, P. Schlenker, R. 1991. Die Mönchsgrasmücke. In : Handbuch der Vögel Mitteleuropas, Vol. 12 (U.N. Glutz von Blotzheim K.M. Bauer, eds pp. 949 1020. Aula, Wiesbaden.
6. Bowers, R.R., Lujan, J., Biboso, A., Kridel, S. Varkey, C. 1994. Premature avian melanocyte death due to low antioxidant levels of protection - fowl model for vitiligo. Pigment Cell Res. 7 : 409 418.
7. Bowers, R.R., Nguyen, B., Buckner, S., Gonzalez, Y. Ruiz, F. 1999. Role of antioxidants in the survival of normal and vitiliginous avian melanocytes. Cell. Mol. Biol. 45 : 1065 1074.
8. Catoni, C., Schaefer, H.M. Peters, A. 2008a. Fruit for health: the effect of flavonoids on humoral immune response and food selection in a frugivorous bird. Funct. Ecol. 22 : 649 654. (Pubitemid 351989285)
9. Catoni, C., Peters, A. Schaefer, H.M. 2008b. Life history trade-offs are influenced by the diversity, availability, and interactions of dietary antioxidants. Anim. Behav. 79 : 1107 1119.
10. Cazetta, E., Schaefer, H.M. Galetti, M. 2009. Why are fruits colorful? The relative importance of achromatic and chromatic contrasts for detection by birds. Evol. Ecol. 23 : 233 244.
11. Corlett, R.T. 1998. Frugivory and seed dispersal by vertebrates in the oriental (Indomalayan) region. Biol. Rev. 73 : 413 448. (Pubitemid 29004896)
12. Cotton, S., Fowler, K. Pomiankowski, A. 2004. Do sexual ornaments demonstrate heightened condition-dependent expression as predicted by the handicap hypothesis? Proc. R. Soc. B 271 : 771 783. (Pubitemid 38491262)
13. Ducrest, A.-L., Keller, L. Roulin, A. 2008. Pleiotropy in the melanocortin system, coloration and behavioural syndromes. Trends Ecol. Evol. 23 : 502.
14. Eggers, S. 2000. Compensatory frugivory in migratory Sylvia warblers: geographical responses to season length. J. Avian Biol. 31 : 63 74. (Pubitemid 30149610)
15. Endler, J. 1990. On the measurement and classification of colour in studies of animal colour patterns. Biol. J. Linn. Soc. 41 : 315 352.
16. Endler, J.A. 1992. Signals, signal conditions, and the direction of evolution. Am. Nat. 139 : S125 S153.
17. Engqvist, L. 2005. The mistreatment of covariate interaction terms in linear model analyses of behavioural and evolutionary ecology studies. Anim. Behav. 70 : 967 971. (Pubitemid 41416642)
18. Fargallo, J.A., Laaksonen, T., Korpimaki, E. Wakamatsu, K. 2007. A melanin-based trait reflects environmental growth conditions of nestling male Eurasian kestrels. Evol. Ecol. 21 : 157 171. (Pubitemid 46318697)
19. Fitze, P.S. Richner, H. 2002. Differential effects of a parasite on ornamental structures based on melanins and carotenoids. Behav. Ecol. 13 : 401 407. (Pubitemid 35249716)
20. Garcia, L.V. 2003. Controlling the false discovery rate in ecological research. Trends Ecol. Evol. 18 : 553 554. (Pubitemid 37240478)
21. Griffith, S.C. 2000. A trade-off between reproduction and a condition-dependent sexually selected ornament in the house sparrow Passer domesticus. Proc. R. Soc. B 267 : 1115 1119. (Pubitemid 30389023)
22. Griffith, S.C., Owens, I.P.F. Burke, T. 1999. Environmental determination of a sexually selected trait. Nature 400 : 358 360. (Pubitemid 29344199)
23. Griffith, S.C., Parker, T.H. Olson, V.A. 2006. Melanin-versus carotenoid-based sexual signals: is the difference really so black and red? Anim. Behav. 71 : 749 763.
24. Guilford, T. Dawkins, M.S. 1991. Receiver psychology and the evolution of animal signals. Anim. Behav. 42 : 1 14.
25. Hart, N.S. Hunt, D.M. 2007. Avian visual pigments: characteristics, spectral tuning, and evolution. Am. Nat. 169 : S7 S26.
26. Hart, N.S. Vorobyev, M. 2005. Modelling oil droplet absorption spectra and spectral sensitivities of bird cone photoreceptors. J. Comp. Physiol. A 191 : 381 392. (Pubitemid 40534198)
27. Hart, N.S., Partridge, J.C., Cuthill, I.C. Bennett, A.T.D. 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. (Pubitemid 30308587)
28. Hasson, O. 1997. Towards a general theory of biological signaling. J. Theor. Biol. 185 : 139 156. (Pubitemid 27158289)
29. Hill, G.E. Brawner, W.R. 1998. Melanin-based plumage coloration in the house finch is unaffected by coccidial infection. Proc. R. Soc. B 265 : 1105 1109. (Pubitemid 28301699)
30. Jawor, J.M. Breitwisch, R. 2003. Melanin ornaments, honesty, and sexual selection. Auk 120 : 249 265. (Pubitemid 36774910)
31. Jordano, P. Herrera, C.M. 1981. The frugivorous diet of blackcap populations Sylvia atricapilla wintering in southern Spain. Ibis 123 : 502 507. (Pubitemid 14273542)
32. Kanter, M., Altan, M.F., Donmez, S., Ocakci, A. Kartal, M.E. 2007. The effects of quercetin on bone minerals, biomechanical behavior, and structure in streptozotocin-induced diabetic rats. Cell Biochem. Funct. 25 : 747 752. (Pubitemid 351202365)
33. Manach, C., Scalbert, A., Morand, C., Remesy, C. Jimenez, L. 2004. Polyphenols: food sources and bioavailability. Am. J. Clin. Nutr. 79 : 727 747. (Pubitemid 41103873)
34. McGraw, K.J. 2003. Melanins, metals, and mate quality. Oikos 102 : 402 406. (Pubitemid 36914282)
35. McGraw, K.J. 2006. Mechanics of melanin-based coloration. In : Bird Coloration: Mechanisms and Measurements, Vol. 1 (G.E. Hill K.J. McGraw, eds pp. 243 294. Harvard University Press, Cambridge.
36. McGraw, K.J. 2007. Dietary mineral content influences the expression of melanin-based ornamental coloration. Behav. Ecol. 18 : 137 142. (Pubitemid 46026323)
37. McGraw, K.J. Hill, G.E. 2000. Differential effects of endoparasitism on the expression of carotenoid- and melanin-based ornamental coloration. Proc. R. Soc. B 267 : 1525 1531. (Pubitemid 30624124)
38. McGraw, K.J., Mackillop, E.A., Dale, J. Hauber, M.E. 2002. Different colors reveal different information: how nutritional stress affects the expression of melanin- and structurally based ornamental plumage. J. Exp. Biol. 205 : 3747 3755. (Pubitemid 36010762)
39. McGraw, K.J., Dale, J. Mackillop, E.A. 2003. Social environment during molt and the expression of melanin- based plumage pigmentation in male house sparrows (Passer domesticus). Behav. Ecol. Sociobiol. 53 : 116 122. (Pubitemid 36708372)
40. McGraw, K.J., Safran, R.J., Evans, M.R. Wakamatsu, K. 2004. European barn swallows use melanin pigments to color their feathers brown. Behav. Ecol. 15 : 889 891. (Pubitemid 39147455)
41. McLachlan, G.J. Chang, S.U. 2004. Mixture modelling for cluster analysis. Stat. Methods Med. Res. 13 : 347 361. (Pubitemid 39405815)
42. Middleton, E., Jr. 1996. Biological properties of plant flavonoids: an overview. Pharm. Biol. 34 : 344 348.
43. Niecke, M., Rothlaender, S. Roulin, A. 2003. Why do melanin ornaments signal individual quality? Insights from metal element analysis of barn owl feathers. Oecologia 137 : 153 158. (Pubitemid 37216111)
44. Ödeen, A. Hastad, O. 2003. Complex distribution of avian color vision systems revealed by sequencing the SWS1 opsin from total DNA. Mol. Biol. Evol. 20 : 855 861. (Pubitemid 36578711)
45. Osorio, D. Ham, A.D. 2002. Spectral reflectance and directional properties of structural coloration in bird plumage. J. Exp. Biol. 205 : 2017 2027. (Pubitemid 34869547)
46. Otte, D. 1974. Effects and functions in the evolution of signaling systems. Annu. Rev. Ecol. Syst. 5 : 385 417.
47. Parrish, J.D. 1997. Patterns of frugivory and energetic condition in nearctic landbirds during autumn migration. Condor 99 : 681 697. (Pubitemid 27353958)
48. Peters, A., Delhey, K., Andersson, S., van Noordwijk, H. Förschler, M.I. 2008. Condition-dependence of multiple carotenoid-based plumage traits: an experimental study. Funct. Ecol. 22 : 831 839.
49. Poston, J.P., Hasselquist, D., Stewart, I.R.K. Westneat, D.F. 2005. Dietary amino acids influence plumage traits and immune responses of male house sparrows, Passer domesticus, but not as expected. Anim. Behav. 70 : 1171 1181. (Pubitemid 41505444)
50. Rohwer, S. Ewald, P.W. 1981. The cost of dominance and advantage of subordination in a badge signaling system. Evolution 35 : 441 454.
51. Roulin, A. 2004a. Covariation between plumage colour polymorphism and diet in the Barn Owl Tyto alba. Ibis 146 : 509 517. (Pubitemid 38908506)
52. Roulin, A. 2004b. The evolution, maintenance and adaptive function of genetic colour polymorphism in birds. Biol. Rev. 79 : 815 848. (Pubitemid 39577124)
53. Roulin, A., Richner, H. Ducrest, A.L. 1998. Genetic, environmental, and condition-dependent effects on female and male ornamentation in the barn owl Tyto alba. Evolution 52 : 1451 1460. (Pubitemid 28537254)
54. Roulin, A., Jungi, T.W., Pfister, H. Dijkstra, C. 2000. Female barn owls (Tyto alba) advertise good genes. Proc. R. Soc. B 267 : 937 941. (Pubitemid 30260996)
55. Roulin, A., Ducret, B., Ravussin, P.A. Altwegg, R. 2003. Female colour polymorphism covaries with reproductive strategies in the tawny owl Strix aluco. J. Avian Biol. 34 : 393 401. (Pubitemid 38098015)
56. Roulin, A., Dauwe, T., Blust, R., Eens, M. Beaud, M. 2006. A link between eumelanism and calcium physiology in the barn owl. Naturwissenschaften 93 : 426 430. (Pubitemid 44222355)
57. Rozanowska, M., Sarna, T., Land, E.J. Truscott, T.G. 1999. Free radical scavenging properties of melanin interaction of eu- and pheo-melanin models with reducing and oxidising radicals. Free Radic. Biol. Med. 26 : 518 525. (Pubitemid 29146254)
58. Schaefer, H.M., Levey, D.J., Schaefer, V. Avery, M.L. 2006. The role of chromatic and achromatic signals for fruit detection by birds. Behav. Ecol. 17 : 784 789. (Pubitemid 44284241)
59. Schaefer, H.M., Schaefer, V. Vorobyev, M. 2007. Are fruit colors adapted to consumer vision and birds equally efficient in detecting colorful signals? Am. Nat. 169 : 159 169.
60. von Schantz, T., Bensch, S., Grahn, M., Hasselquist, D. Wittzell, H. 1999. Good genes, oxidative stress and condition-dependent sexual signals. Proc. R. Soc. B 266 : 1 12. (Pubitemid 29039269)
61. Schluter, D. Price, T. 1993. Honesty, perception and population divergence in sexually selected traits. Proc. R. Soc. B 253 : 117 122.
62. Schwarz, M., Hillebrand, S., Habben, S., Degenhardt, A. Winterhalten, P. 2003. Application of high-speed countercurrent chromatography to the large-scale isolation of anthocyanins. Biochem. Eng. J. 14 : 179 189. (Pubitemid 36569229)
63. Searcy, W.A. Nowicki, S. 2005. The Evolution of Animal Communication: Reliability and Deception in Signaling Systems. Princeton University Press, Princeton, NJ.
64. Shirihai, H., Gargallo, G. Helbig, A.J. 2001. Sylvia Warblers: Identification, Taxonomy and Phylogeny of the Genus Sylvia. A. & C. Black, London.
65. Siddiqi, A., Cronin, T.W., Loew, E.R., Vorobyev, M. Summers, K. 2004. Interspecific and intraspecific views of color signals in the strawberry poison frog Dendrobates pumilio. J. Exp. Biol. 207 : 2471 2485. (Pubitemid 39009283)
66. Terborgh, J.W. 1986. Community aspects of frugivory in tropical forests. In : Frugivores and Seed Dispersal (A. Estrada T.H. Fleming, eds pp. 371 384. Junk, Dordrecht.
67. Verhoeven, K.J.F., Simonsen, K.L. McIntyre, L.M. 2005. Implementing false discovery rate control: increasing your power. Oikos 108 : 643 647. (Pubitemid 40336053)
68. Vorobyev, M. Osorio, D. 1998. Receptor noise as a determinant of colour thresholds. Proc. R. Soc. B 265 : 351 358. (Pubitemid 28111918)
69. Vorobyev, M., Osorio, D., Bennett, A.T.D., Marshall, N.J. Cuthill, I.C. 1998. Tetrachromacy, oil droplets and bird plumage colours. J. Comp. Physiol. A 183 : 621 633. (Pubitemid 28554072)
70. Yamaguchi, M., Hamamoto, R., Uchiyama, S. Ishiyama, K. 2007. Effects of flavonoid on calcium content in femoral tissue culture and parathyroid hormone-stimulated osteoclastogenesis in bone marrow culture ntro. Mol. Cell. Biochem. 303 : 83 88. (Pubitemid 47261304)