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Testosterone and melanin-based black plumage coloration: a comparative study

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Abstract

Despite the functional significance of melanin-based plumage coloration in social and sexual signaling, the mechanisms controlling its information content are poorly understood. The T-regulation hypothesis proposes that melanin ornaments signal competitive abilities via the effects of testosterone (T) mediating both melanization and sexual/aggressive behaviors. Using the phylogenetic comparative approach, we tested whether frontal black melanization is associated with elevated T around the time of breeding plumage development across all bird species with available T-data. We found a context-dependent relationship between melanization and T, varying with the type of ornamentation (patchy or full-black) and with the presumed taxonomic distribution of the hormonal control of plumage dichromatism. Within two taxa in which male plumage development is assumed androgen-dependent (Charadriiformes, Corvida), evolutionary increases in male melanization, and melanin dichromatism correlated with increases in T in most analyses but not within the basal lineage (ratites, Galloanseriformes) with androgen-independent male plumage. Among Passeroidea with presumably genetically or luteinizing-hormone-based male plumage, melanization and its dichromatism correlated with T only in species with <100% frontal melanization. These results were robust as we controlled for several confounding variables such as mating and parental behaviors. This study is the first to test and support the T-regulation hypothesis interspecifically, suggesting that among-species differences in melanization may have evolved in response to differences in circulating T in certain avian taxa. Our results imply that the extent of black ornamentation may serve as an honest indicator of male competitiveness in those species that evolved an appropriate hormonal basis (T dependence) for color production.

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References

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

    Google Scholar 

  • Barker FK, Cibois A, Schikler P, Feinstein J, Cracraft J (2004) Phylogeny and diversification of the largest avian radiation. Proc Natl Acad Sci U S A 101:11040–11045

    Article  PubMed  CAS  Google Scholar 

  • Bennett PM, Owens IPF (2002) Evolutionary ecology of birds: life histories, mating systems and extinction. Oxford University Press, Oxford

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Bókony V, Liker A (2005) Melanin-based black plumage coloration is related to reproductive investment in cardueline finches. Condor 107:775–787

    Article  Google Scholar 

  • Bókony V, Liker A, Székely T, Kis J (2003) Melanin-based plumage coloration and flight displays in plovers and allies. Proc R Soc Lond B 270:2491–2497

    Article  Google Scholar 

  • Brawner WR, Hill GE, Sundermann CA (2000) Effects of coccidial and mycoplasmal infections on carotenoid-based plumage pigmentation in male House Finches. Auk 117:952–963

    Article  Google Scholar 

  • Buchanan KL, Evans MR, Goldsmith AR, Bryan DM, Rowe LV (2001) Testosterone influences basal metabolic rate in male house sparrows: a new cost of dominance signalling? Proc R Soc Lond B 268:1337–1344

    Article  CAS  Google Scholar 

  • Burtt EH, Ichida JM (2004) Gloger’s rule, feather-degrading bacteria, and color variation among song sparrows. Condor 106:681–686

    Article  Google Scholar 

  • Carefoot WC (2002) Hen-feathering mutation HF*H may act as a eumelanising factor and modify the expression of autosomal barring. Br Poult Sci 43:391–394

    Article  PubMed  CAS  Google Scholar 

  • Cohen J (1988) Statistical power analysis for the behavioural sciences. Erlbaum, Hillsdale

    Google Scholar 

  • Doucet SM, Shawkey MD, Hill GE, Montgomerie R (2006) Iridescent plumage in satin bowerbirds: structure, mechanisms and nanostructural predictors of individual variation in colour. J Exp Biol 209:380–390

    Article  PubMed  Google Scholar 

  • Edwards PJ (1982) Plumage variation, territoriality and breeding displays of the golden plover Pluvialis apricaria in Southwest Scotland. Ibis 124:88–95

    Article  Google Scholar 

  • 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 47:156–163

    Article  Google Scholar 

  • Fargallo JA, Laaksonen T, Korpimäki E, Wakamatsu K (2007a) A melanin-based trait reflects environmental growth conditions of nestling male Eurasian kestrels. Evol Ecol 21:157–171

    Article  Google Scholar 

  • Fargallo JA, Martínez-Padilla J, Toledano-Díaz A, Santiago-Moreno J, Dávila JA (2007b) Sex and testosterone effects on growth, immunity and melanin coloration of nestling Eurasian kestrels. J Anim Ecol 76:201–209

    Article  PubMed  Google Scholar 

  • Fitze PS, Richner H (2002) Differential effects of a parasite on ornamental structures based on melanins and carotenoids. Behav Ecol 13:401–407

    Article  Google Scholar 

  • Freckleton RP, Harvey PH, Pagel M (2002) Phylogenetic analysis and comparative data: a test and review of evidence. Am Nat 160:712–726

    Article  PubMed  CAS  Google Scholar 

  • Garamszegi LZ (2006) Comparing effect sizes across variables: generalization without the need for Bonferroni correction. Behav Ecol 17:682–687

    Article  Google Scholar 

  • Garamszegi LZ, Eens M, Hurtrez-Boussès S, Møller AP (2005) Testosterone, testes size and mating success in birds: a comparative study. Horm Behav 47:389–409

    Article  PubMed  CAS  Google Scholar 

  • González G, Sorci G, Smith LC, de Lope F (2001) Testosterone and sexual signalling in male House Sparrows (Passer domesticus). Behav Ecol Sociobiol 50:557–562

    Google Scholar 

  • Goymann W, Moore IT, Scheuerlein A, Hirschenhauser K, Grafen A, Wingfield JC (2004) Testosterone in tropical birds: effects of environmental and social factors. Am Nat 164:327–334

    Article  PubMed  Google Scholar 

  • Grafen A, Hails R (2002) Modern statistics for the life sciences. Oxford University Press, Oxford

    Google Scholar 

  • Griffith SC, Owens IPF, Burke T (1999) Environmental determination of a sexually selected trait. Nature 400:358–360

    Article  CAS  Google Scholar 

  • Griffith SC, Parker TH, Olson VA (2006) Melanin- versus carotenoid-based sexual signals: is the difference really so black and red? Anim Behav 71:749–763

    Article  Google Scholar 

  • Haase E, Schmedemann R (1992) Dose-dependent effect of testosterone on the induction of eclipse coloration in castrated wild mallard drakes (Anas platyrhynchos L.). Can J Zool 70:428–431

    Article  Google Scholar 

  • Haase E, Ito S, Wakamatsu K (1995) Influences of sex, castration, and androgens on the eumelanin and pheomelanin contents of different feathers in wild Mallards. Pigment Cell Res 8:164–170

    Article  PubMed  CAS  Google Scholar 

  • Hegner RE, Wingfield JC (1987) Effects of experimental manipulation of testosterone levels on parental investment and breeding success in male house sparrows. Auk 104:462–469

    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 (2006) Female mate choice for ornamental coloration. In: Hill GE, McGraw KJ (eds) Bird coloration II. Function and evolution. Harvard University Press, Cambridge, pp 137–200

    Google Scholar 

  • Hill GE, Montgomerie R (1994) Plumage colour signals nutritional condition in the house finch. Proc R Soc Lond B 258:47–52

    Article  Google Scholar 

  • Hill GE, Brawner WR (1998) Melanin-based plumage coloration in the House Finch is unaffected by coccidial infection. Proc R Soc Lond B 265:1105–1109

    Article  Google Scholar 

  • Hill GE, McGraw KJ (2003) Melanin, nutrition, and the lion’s mane. Science (Lett) 299:660

    Article  Google Scholar 

  • Hirschenhauser K, Winkler H, Oliveira RF (2003) Comparative analysis of male androgen responsiveness to social environment in birds: the effects of mating system and paternal incubation. Horm Behav 43:508–519

    Article  PubMed  CAS  Google Scholar 

  • Jawor JM, Breitwisch R (2003) Melanin ornaments, honesty, and sexual selection. Auk 120:249–265

    Article  Google Scholar 

  • Ketterson ED, Nolan V Jr, Sandell M (2005) Testosterone in females: mediator of adaptive traits, constraint on sexual dimorphism, or both? Am Nat 166:S85–98

    Article  PubMed  Google Scholar 

  • Kimball RT (2006) Hormonal control of coloration. In: Hill GE, McGraw KJ (eds) Bird coloration I. Mechanisms and measurements. Harvard University Press, Cambridge, pp 137–200

    Google Scholar 

  • Kimball RT, Ligon JD (1999) Evolution of avian plumage dichromatism from a proximate perspective. Am Nat 154:182–193

    Article  Google Scholar 

  • Lendvai AZ, Kis J, Székely T, Cuthill IC (2004) An investigation of mate choice based on manipulation of multiple ornaments in Kentish Plovers. Anim Behav 67:703–709

    Article  Google Scholar 

  • Liker A, Székely T (2005) Mortality costs of sexual selection and parental care in natural populations of birds. Evolution 59:890–897

    PubMed  Google Scholar 

  • Mahler B, Araujo LS, Tubaro PL (2003) Dietary and sexual correlates of carotenoid pigment expression in dove plumage. Condor 105:258–267

    Article  Google Scholar 

  • Martins EP, Hansen TF (1997) Phylogenies and the comparative method: a general approach to incorporating phylogenetic information into the analysis of interspecific data. Am Nat 149:646–667

    Article  Google Scholar 

  • McGraw KJ (2003) Melanins, metals, and mate quality. Oikos 102:402–406

    Article  CAS  Google Scholar 

  • McGraw KJ (2006) Mechanics of melanin-based coloration. In: Hill GE, McGraw KJ (eds) Bird coloration I. Mechanisms and measurements. Harvard University Press, Cambridge, pp 243–294

    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, Vonnegut EA, Dale J, Hauber ME (2002) Different plumage colors reveal different information: how nutritional stress affects the expression of melanin- and structurally based ornamental coloration. J Exp Biol 205:3747–3755

    PubMed  Google Scholar 

  • McGraw KJ, Dale J, Mackillop EA (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

    Google Scholar 

  • McGraw KJ, Wakamatsu K, Ito S, Nolan PM, Jouventin P, Dobson FS, Austic RE, Safran RJ, Siefferman LM, Hill GE, Parker RS (2004) You can’t judge a pigment by its color: carotenoid and melanin content of yellow and brown feathers in swallows, bluebirds, penguins, and domestic chickens. Condor 106:390–395

    Article  Google Scholar 

  • Møller AP, Jennions MD (2002) How much variance can be explained by ecologists and evolutionary biologists? Oecologia 132:492–500

    Article  Google Scholar 

  • Møller AP, Garamszegi LZ, Gil D, Hurtrez-Boussès S, Eens M (2005) Correlated evolution of male and female testosterone profiles in birds and its consequences. Behav Ecol Sociobiol 58:534–544

    Article  Google Scholar 

  • Nakagawa S (2004) A farewell to Bonferroni: the problems of low statistical power and publication bias. Behav Ecol 15:1044–1045

    Article  Google Scholar 

  • Olson VA, Owens IPF (2005) Interspecific variation in the use of carotenoid-based coloration in birds: diet, life history and phylogeny. J Evol Biol 18:1534–1546

    Article  PubMed  CAS  Google Scholar 

  • Owens IPF, Hartley IR (1998) Sexual dimorphism in birds: why are there so many different forms of dimorphism? Proc R Soc Lond B 265:397–407

    Article  Google Scholar 

  • Owens M (1997) Inferring evolutionary processes from phylogenies. Zool Scripta 26:331–348

    Article  Google Scholar 

  • Pagel M (1999) Inferring the historical patterns of biological evolution. Nature 401:877–884

    Article  PubMed  CAS  Google Scholar 

  • Peters A, Astheimer LB, Boland CRJ, Cockburn A (2000) Testosterone is involved in acquisition and maintenance of sexually selected male plumage in superb fairy-wrens, Malurus cyaneus. Behav Ecol Sociobiol 47:438–445

    Article  Google Scholar 

  • Poston JP, Hasselquist D, Stewart IRK, Westneat DF (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

    Article  Google Scholar 

  • Roberts ML, Buchanan KL, Evans MR (2004) Testing the immunocompetence handicap hypothesis: a review of the evidence. Anim Behav 68:227–239

    Article  Google Scholar 

  • Roulin A, Dijkstra C (2003) Genetic and environmental components of variation in eumelanin and phaeomelanin sex-traits in the barn owl. Heredity 90:359–364

    Article  PubMed  CAS  Google Scholar 

  • Roulin A, Riols C, Dijkstra C, Ducrest A-L (2001) Female plumage spottiness signals parasite resistance in the barn owl (Tyto alba). Behav Ecol 12:103–110

    Article  Google Scholar 

  • Roulin A, Müller W, Sasvári L, Dijkstra C, Ducrest AL, Riols C, Wink M, Lubjuhn T (2004) Extra-pair paternity, testes size and testosterone level in relation to colour polymorphism in the barn owl Tyto alba. J Avian Biol 35:492–500

    Article  Google Scholar 

  • Senar JC (2006) Color displays as intrasexual signals of aggression and dominance. In: Hill GE, McGraw KJ (eds) Bird coloration II. Function and evolution. Harvard University Press, Cambridge, pp 87–136

    Google Scholar 

  • Sibley CG, Ahlquist JE (1990) Phylogeny and classification of birds: a study in molecular evolution. Yale University Press, New Haven

    Google Scholar 

  • Wingfield JC, Ball GF, Duffy AM Jr, Hegner RE, Ramenofsky M (1987) Testosterone and aggression in birds. Am Sci 75:602–608

    Google Scholar 

  • Wingfield JC, Hegner RE, Dufty AM Jr, Ball GF (1990) The ‘challenge hypothesis’: theoretical implications for patterns of testosterone secretion, mating systems and breeding strategies. Am Nat 136:829–846

    Article  Google Scholar 

  • Wingfield JC, Lynn SE, Soma KK (2001) Avoiding the ‘costs’ of testosterone: ecological bases of hormone-behavior interactions. Brain Behav Ecol 57:239–251

    Article  CAS  Google Scholar 

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Acknowledgments

We thank four anonymous referees for valuable comments on the manuscript. VB and AL were supported by the Hungarian Scientific Research Fund (OTKA, T047256), VB by an Eötvös scholarship from the Hungarian Scholarship Board (MÖB), and AL by a Bolyai János Research Fellowship. LZG received a post-doc grant from FWO, Vlaanderen (Belgium). KH was supported by a post-doctoral grant from the Fundação para a Ciência e a Tecnologia (PRAXIS XI/BPD/20142/99), and a research grant to R. F. Oliveira, ISPA, Lisbon, Portugal (FCT; PRAXIS XXI/P/BIA/10251/98).

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Correspondence to Veronika Bókony.

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Communicated by: K. McGraw

Electronic supplementary material

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S1

Reliability of species-specific T measures used in the study (DOC 31 kb)

S2

Data on melanization, T levels, and confounding variables used in the analyses (DOC 397 kb)

S3

Topology and references of the composite phylogenies used in the analyses (DOC 431 KB)

S4

Full multivariate phylogenetic GLS models of male melanization and melanin dichromatism in relation to T levels and sexual and paternal behaviors (DOC 70 kb)

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Bókony, V., Garamszegi, L.Z., Hirschenhauser, K. et al. Testosterone and melanin-based black plumage coloration: a comparative study. Behav Ecol Sociobiol 62, 1229–1238 (2008). https://doi.org/10.1007/s00265-008-0551-2

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  • DOI: https://doi.org/10.1007/s00265-008-0551-2

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