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Male pheomelanin pigmentation and breeding onset in Barn Swallows Hirundo rustica gutturalis

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Abstract

Plumage color is a composite trait and each component can provide information regarding individual quality. Melanin-based color is one of the most common plumage coloration in birds. This color comprises two types of melanin pigments: eumelanin (black pigment) and pheomelanin (yellow-reddish pigment), and it is affected by several post-molting processes such as UV damage, staining, and preen oils. In some birds, pheomelanin-based plumage color is related to several measures of sexual selection; however, pheomelanin is almost always expressed together with eumelanin and affected by post-molting processes. Therefore, it is still unclear whether (and to what extent) pheomelanin can explain the observed relationship between plumage color and the measure of sexual selection. Here we examined the melanin (both eumelanin and pheomelanin) concentration in relation to breeding onset, as a fitness component associated with sexual selection in male Barn Swallows (Hirundo rustica gutturalis). We found that throat feathers in males contained more pheomelanin than those in females. The amount of pheomelanin, but not eumelanin, declined throughout the sampling period, indicating that pheomelanin pigmentation conveys different information than eumelanin. Even after correcting for depigmentation of melanin, males with more pheomelanin bred earlier than the others. Together with the results from previous studies, these findings indicate that pheomelanin-based coloration may have evolved via sexual selection for pheomelanin pigmentation in Barn Swallows.

Zusammenfassung

Phäomelanin Pigmentierung bei männlichen Rauchschwalben ( Hirundo rustica gutturalis ) und Brutbeginn

Gefiederfärbung ist eine vielteilige Eigenschaft, und jede Komponente kann Informationen liefern über die Qualität eines Individuums. Melanin-Färbung ist eine der häufigsten Gefiederfärbungen bei Vögeln. Diese Farbe besteht aus zwei Typen des Melanin-Pigments: Eumelanin (schwarz) und Phäomelanin (gelb-rötlich), und unterliegt verschiedenen weiteren Veränderungen nach der Mauser, wie Schädigung durch UV-Strahlung, Schmutz und Bürzeldrüsenfett. Bei manchen Vögeln hängt eine Phäomelanin-Färbung zusammen mit verschiedenen Maßen der sexuellen Auslese; allerdings wird Phäomelanin fast immer zusammen mit Eumelanin gebildet und ist von Einwirkungen nach der Mauser betroffen. Daher ist es noch immer unklar, ob und inwieweit Phäomelanin die beobachteten Zusammenhänge zwischen Gefiederfärbung und den Maßen der sexuellen Auslese erklären kann. Hier untersuchten wir die Melaninkonzentration im Vergleich zum Brutbeginn als Fitness-Merkmal im Zusammenhang mit sexueller Auslese bei männlichen Rauchschwalben (Hirundo rustica gutturalis). Wir fanden, dass Kehlfedern bei Männchen mehr Phäomelanin enthielten als bei Weibchen. Die Menge an Phäomelanin, aber nicht Eumelanin, nahm über den Zeitraum der Untersuchung ab, was darauf hindeutet, dass die Phäomelanin-Färbung andere Informationen vermittelt als die Eumelanin-Färbung. Selbst nach einer Korrektur für die Entfärbung des Melanin, begannen Männchen mit mehr Phäomelanin früher mit dem Brüten. Zusammen mit Ergebnissen aus früheren Untersuchungen, deuten diese Erkenntnisse darauf hin, dass Phäomelanin-Färbung bei Rauchschwalben sich über sexuelle Selektion entwickelt haben könnten.

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References

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

    Google Scholar 

  • Arai E, Hasegawa M, Nakamura M (2009) Divorce and asynchronous arrival in Barn Swallows Hirundo rustica. Bird Study 56:411–413

  • Bonser RHC (1995) Melanin and the abrasion resistance of feathers. Condor 97:590–591

    Article  Google Scholar 

  • Chedekel MR, Smith SK, Post PW, Pokora A, Vessell DL (1978) Photodestruction of pheomelanin: role of oxygen. Proc Natl Acad Sci USA 75:5395–5399

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cramp S (1988) The birds of the Western Palearctic, vol 5. Oxford University Press, Oxford

    Google Scholar 

  • Da Silva A, van den Brink V, Emaresi G, Luzio E, Bize P, Dreiss AN, Roulin A (2013) Melanin-based colour polymorphism signals aggressive personality in nest and territory defence in the tawny owl (Strix aluco). Behav Ecol Sociobiol 67:1041–1052

    Article  Google Scholar 

  • Delhey K, Burger C, Fiedler W, Peters A (2010) Seasonal changes in colour: a comparison of structural, melanin- and caronenoid-based plumage colours. PLoS ONE 5(7):e11582

    Article  PubMed Central  PubMed  Google Scholar 

  • Ducrest AL, Keller L, Roulin A (2008) Pleiotropy in the melanocortin system, coloration and behavioural syndromes. Trends Ecol Evol 23:502–510

    Article  PubMed  Google Scholar 

  • Emaresi G, Ducrest AL, Bize P, Richter H, Simon C, Roulin A (2013) Pleiotropy in the melanocortin system: expression levels of this system are associated with melanogenesis and pigmentation in the tawny owl (Strix aluco). Mol Ecol 22:4915–4930

    Article  CAS  PubMed  Google Scholar 

  • Enstrom DA (1993) Female choice for age-specific plumage in the orchard oriole: implications for delayed plumage maturation. Anim Behav 45:435–442

    Article  Google Scholar 

  • Figuerola J, Senar JC (2005) Seasonal changes in carotenoid- and melanin-based plumage coloration in the Great Tit Parus major. Ibis 147:797–802

    Article  Google Scholar 

  • Foley JD, van Dam A (1984) Intensity and color. In: Foley JD, van Dam A (eds) Fundamentals of interactive computer graphics. Addison-Wesley, Boston, pp 593–622

    Google Scholar 

  • Galván I (2010) Plumage coloration can be perceived as a multiple condition-dependent signal by Great Tits Parus major. Ibis 152:359–367

    Article  Google Scholar 

  • Galván I, Møller AP (2009) Different roles of natural and sexual selection on senescence of plumage colour in the barn swallow. Funct Ecol 23:302–309

    Article  Google Scholar 

  • Galván I, Møller AP (2013) Pheomelanin-based plumage coloration predicts survival rates in birds. Physiol Biochem Zool 86:184–192

    Article  PubMed  Google Scholar 

  • Galván I, Bijlsma RG, Negro JJ, Jarén M, Garrido-Fernández J (2010) Environmental constraints for plumage melanization in the northern goshawk Accipiter gentilis. J Avian Biol 41:523–531

    Article  Google Scholar 

  • Galván I, Ghanem I, Møller AP (2012) Has removal of excess cycteine led to the evolution of pheomelanin? BioEssay 34:565–568

    Article  Google Scholar 

  • Grüebler MU, Naef-Daenzer B (2010) Fitness consequences of timing of breeding in birds: data effects in the course of a reproductive episode. J Avian Biol 41:282–291

    Article  Google Scholar 

  • Gunderson AR, Forsyth MH, Swaddle JP (2009) Evidence that plumage bacteria influence feather coloration and body condition of eastern bluebirds Sialia sialis. J Avian Biol 40:440–447

    Article  Google Scholar 

  • Haase E, Ito S, Sell A, Wakamatsu K (1992) Melanin concentrations in feathers from wild and domestic pigeons. J Hered 83:64–67

    CAS  Google Scholar 

  • Hasegawa M (2011) Sexual selection on multiple ornaments in the Barn Swallow Hirundo rustica gutturalis. PhD thesis, University of Tsukuba, Tsukuba

  • Hasegawa M, Arai E, Watanabe M, Nakamura M (2008) Methods for correcting plumage color fading in the Barn Swallow. Ornithol Sci 7:117–122

    Article  Google Scholar 

  • Hasegawa M, Arai E, Watanabe M, Nakamura M (2010a) Mating advantage of multiple male ornaments in the Barn Swallow Hirundo rustica gutturalis. Ornithol Sci 9:141–148

    Article  Google Scholar 

  • Hasegawa M, Arai E, Kojima W, Kitamura W, Fujita G, Higuchi H, Watanabe M, Nakamura M (2010b) Low level of extra-pair paternity in a population of the Barn Swallow Hirundo rustica gutturalis. Ornithol Sci 9:161–164

    Article  Google Scholar 

  • Hill GE (2006) Chapter 4: Female mate choice for ornamental coloration. In: Hill GE, McGraw KJ (eds) Bird coloration, vol 2. Function and evolution. Harvard University Press, Cambridge, pp 137–200

    Google Scholar 

  • Hill HZ, Hill GL (2000) UVA, pheomelanin and the carcinogenesis of melanoma. Pigment Cell Res 13(Suppl 8):140–144

    Article  PubMed  Google Scholar 

  • Hoting E, Zimmermann M, Hocker H (1995) Photochemical alterations in human hair. Part II: analysis of melanin. J Soc Cosmet Chem 46:181–190

    CAS  Google Scholar 

  • Ito S, Nakanishi Y, Valezuela RK, Brilliant MH, Kolbe L, Wakamatsu K (2011) Usefulness of alkaline hydrogen peroxide oxidation to analyze eumelanin and pheomelanin in various tissue samples: application to chemical analysis of human hair melanins. Pigment Cell Melanoma Res 24:605–613

    Article  CAS  PubMed  Google Scholar 

  • Jacob J, Eigener U, Hoppe U (1997) The structure of preen gland waxes from pelecaniform birds containing 3,7-dimethyloctan-1-ol—an active ingredient against dermatophytes. Z Naturforsch C 52:114–123

    CAS  Google Scholar 

  • Jenkins BR, Vitousek MN, Safran RJ (2013) Signaling stress? An analysis of pheomelanin-based plumage color and individual corticosticosterone levels at two temporal scales in North American barn swallows, Hirundo rustica erythrogaster. Horm Behav 64:665–672

    Article  CAS  PubMed  Google Scholar 

  • Laczi M, Hegyi G, Herényi M, Kiss D, Markó G, Nagy G, Rosivall B, Szöllősi E, Török J (2013) Integrated plumage colour variation in relation to body condition, reproductive investment and laying date in the collared flycatcher. Naturwissenschften 100:983–991

    Article  CAS  Google Scholar 

  • Lendvai JK, Kis J, Szekely 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 

  • López-Rull I, Pagán I, Garcia CM (2010) Cosmetic enhancement of signal coloration: experimental evidence in the house finch. Behav Ecol 21:781–787

    Article  Google Scholar 

  • McGraw KJ, Hill GE (2004) Plumage color as a dynamic trait: carotenoid pigmentation of male House Finches (Carpodacus mexicanus) fades during the breeding season. Can J Zool 82:734–738

    Article  Google Scholar 

  • McGraw KJ, Mackillop EA, Dale J, Hauber ME (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

    PubMed  Google Scholar 

  • McGraw KJ, Safran RJ, Evans MR, Wakamatsu K (2004) European barn swallows use melanin pigments to color their feathers brown. Behav Ecol 15:889–891

    Article  Google Scholar 

  • McGraw KJ, Safran RJ, Wakamatsu K (2005) How feather color reflects its melanin content. Funct Ecol 19:816–821

    Article  Google Scholar 

  • Møller AP (1994) Phenotype-dependent arrival time and its consequences in migratory bird. Behav Ecol Sociobiol 35:115–122

    Article  Google Scholar 

  • Møller AP, Chabi Y, Cuervo JJ, de Lope F, Kilpimaa J, Kose M et al (2006) An analysis of continent-wide patterns of sexual selection in a passerine bird. Evolution 60:856–868

  • Omland KE (1996) Female mallard mating preferences for multiple male ornaments. I. Natural variation. Behav Ecol Sociobiol 39:353–360

    Article  Google Scholar 

  • Ozeki H, Wakamatsu K, Ito S (1997) Chemical characterization of eumelanins with special emphasis on 5,6-dihydroxyindole-2-carboxylic acid content and molecular size. Anal Biochem 248:149–157

    Article  CAS  PubMed  Google Scholar 

  • Palokangas P, Korpimäki E, Hakkarainen H, Huhta E, Tolonen P, Alatalo RV (1994) Female kestrels gain reproductive success by choosing brightly ornamented males. Anim Behav 12:443–448

    Article  Google Scholar 

  • Perez-Rodriguez L, Mougeot F, Bortolotti GR (2011) The effects of preen oils and soiling on the UV–visible reflectance of carotenoid-pigmented feathers. Behav Ecol Sociobiol 65:1425–1435

    Article  Google Scholar 

  • Piersma T, Dekker M, Sinninghe Damste JS (1999) An avian equivalent of make-up? Ecol Lett 2:201–203

    Article  Google Scholar 

  • R Development Core Team (2008) R: alanguage and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

  • Roulin A, Ducrest AL (2011) Association between melanism, physiology and behaviour: a role for the melanocortin system. Eur J Pharmacol 660:226–233

    Article  CAS  PubMed  Google Scholar 

  • Roulin A, Gasparini J, Bize P, Ritschard M, Richner H (2008) Melanin-based colorations signal strategies to cope with poor and rich environments. Behav Ecol Sociobiol 62:507–519

    Article  Google Scholar 

  • Roulin A, Almasi B, Meichtry-Stier KS, Jenni L (2011a) Eumelanin- and pheomelanin-based colour advertise resistance to oxidative stress in opposite ways. J Evol Biol 24:2241–2247

    Article  CAS  PubMed  Google Scholar 

  • Roulin A, Emaresi G, Bize P, Gasparini J, Piault R, Ducrest AL (2011b) Pale and dark reddish melanic tawny owls differentially regulate the level of blood circulating POMC prohormone in relation to environmental conditions. Oecologia 166:913–921

    Article  PubMed  Google Scholar 

  • Safran RJ, McGraw KJ (2004) Plumage coloration, not length or symmetry of tail-streamers, is a sexually selected trait in North American barn swallows. Behav Ecol 15:455–461

    Article  Google Scholar 

  • Safran RJ, McGraw KJ, Wilkins MR, Hubbard JH, Marling J (2010) Positive carotenoid balance correlates with greater reproductive performance in a wild bird. PLoS ONE 5:e9420

    Article  PubMed Central  PubMed  Google Scholar 

  • Saino N, Romano M, Rubolini D, Teplisky C, Ambrosini R, Caprioli M, Canova L, Wakamatsu K (2013a) Sexual dimorphism in melanin pigmentation, feather coloration and its heritability in the Barn Swallow (Hirundo rustica). PLoS ONE 8(2):e58024. doi:10.1371/journal.pone.0058024

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Saino N, Canova L, Costanzo A, Rubolini D, Roulin A, Møller AP (2013b) Immune and stress responses covary with melanin-based coloration in the barn swallow. Evol Biol 40:521–531

    Article  Google Scholar 

  • Shawkey MD, Pillai SR, Hill GE (2003) Chemical warfare? Effects of uropygial oil on feather-degrading bacteria. J Avian Biol 34:345–349

    Article  Google Scholar 

  • Shawkey MD, Pillai SR, Hill GE, Siefferman LM, Roberts SR (2007) Bacteria as an agent for change in structural plumage color: correlational and experimental evidence. Am Nat 169:S112–S121

    Article  PubMed  Google Scholar 

  • Shawkey MD, Pillai SR, Hill GE (2009) Do feather degrading bacteria affect sexually selected plumage color? Naturwissenschaften 96:123–128

    Article  CAS  PubMed  Google Scholar 

  • Siefferman L, Hill GE (2003) Structural and melanin plumage coloration indicate parental effort and reproductive success in male eastern bluebirds. Behav Ecol 14:855–861

    Article  Google Scholar 

  • Surmacki A (2008) Preen waxes do not protect carotenoid plumage from bleaching by sunlight. Ibis 150:335–341

    Article  Google Scholar 

  • Surmacki A, Nowakowski JK (2007) Soil and preen waxes influence the expression of carotenoid-based plumage coloration. Naturwissenschaften 94:829–835

    Article  CAS  PubMed  Google Scholar 

  • Tajima K, Nakamura M (2003) Response to manipulation of partner contribution: a handicapping experiment in the Barn Swallow. Ornithol Sci 2:65–72

    Article  Google Scholar 

  • Turner AK  (2006) The barn swallow. Poyser, London

  • Vitousek MN, Stewart RA, Safran RJ (2013) Female plumage colour influences seasonal oxidative damage and testosterone profiles in a songbird. Biol Lett 9(5):20130539

    Article  PubMed Central  PubMed  Google Scholar 

  • Vortman Y, Lotem A, Dor R, Lovette IJ, Safran RJ (2011) The sexual signals of the East-Mediterranean barn swallow: a different swallow tale. Behav Ecol 22:1344–1352

    Article  Google Scholar 

  • Vortman Y, Lotem A, Dor R, Lovette I, Safran RJ (2013) Multiple sexual signals and behavioral reproductive isolation in a diverging population. Am Nat 184:514–523

    Article  Google Scholar 

  • Wakamatsu K, Ito S, Rees JL (2002) The usefulness of 4-amino-3-hydroxyphenylalanine as a specific marker of pheomelanin. Pigment Cell Res 15:225–232

    Article  CAS  PubMed  Google Scholar 

  • Williams TD (2012) Chapter 3: Timing of Breeding. In: Williams TD (ed) Physiological adaptations for breeding in birds. Princeton University Press, Princeton, pp 52–99

    Google Scholar 

  • Willoughby EJ, Murphy M, Gorton HL (2002) Molt, plumage abrasion, and color change in Lawrence’s Goldfinch. Wilson Bull 114:380–392

    Article  Google Scholar 

  • Zampiga E, Hoi H, Pllastro A (2004) Preening, plumage reflectance and female choice in budgerigars. Ethol Ecol Evol 16:339–349

    Article  Google Scholar 

  • Zuk M, Johnson K, Thornhill R, Ligon JD (1990) Mechanisms of mate choice in red jungle fowl. Evolution 44:477–485

    Article  Google Scholar 

Download references

Acknowledgments

We are grateful to the residents of Joetsu City for their kind support and assistance. We thank the members of the Department of Chemistry, School of Health Sciences, Fujita Health University, the Laboratory of Animal Ecology of Joetsu University of Education, the Laboratory of Ecology and Evolutionary Biology of Tohoku University and Innocence Plus English school. We also express our thanks to Shosuke Ito, Mamoru Watanabe and Yuma Takahashi for their useful suggestions.

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Authors and Affiliations

  1. Division of Ecology and Evolutionary Biology, Graduate School of Life Sciences, Tohoku University, Biological Buildings, Aoba, Sendai, 980-8578, Japan

    Emi Arai

  2. Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, 1-1-1 Tennoudai, Tsukuba, Ibaraki, 305-8572, Japan

    Masaru Hasegawa

  3. Laboratory of Animal Ecology, Department of Biology, Joetsu University of Education, 1 Yamayashiki-machi, Joetsu, Niigata, 943-8512, Japan

    Masahiko Nakamura

  4. Department of Chemistry, Fujita Health University School of Health Sciences, Toyoake, Aichi, 470-1192, Japan

    Kazumasa Wakamatsu

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  1. Emi Arai
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  2. Masaru Hasegawa
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  3. Masahiko Nakamura
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  4. Kazumasa Wakamatsu
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Correspondence to Emi Arai.

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Communicated by K. C. Klasing.

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Arai, E., Hasegawa, M., Nakamura, M. et al. Male pheomelanin pigmentation and breeding onset in Barn Swallows Hirundo rustica gutturalis . J Ornithol 156, 419–427 (2015). https://doi.org/10.1007/s10336-014-1140-y

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