Advertisement

Journal of Comparative Physiology B

, Volume 189, Issue 3–4, pp 441–450 | Cite as

Pheomelanin synthesis varies with protein food abundance in developing goshawks

  • Ismael GalvánEmail author
  • Alberto Jorge
  • Jan T. Nielsen
  • Anders P. Møller
Original Paper

Abstract

The accumulation of the amino acid cysteine in lysosomes produces toxic substances, which are avoided by a gene (CTNS) coding for a transporter that pumps cystine out of lysosomes. Melanosomes are lysosome-related organelles that synthesize melanins, the most widespread pigments in animals. The synthesis of the orange melanin, termed pheomelanin, depends on cysteine levels because the sulfhydryl group is used to form the pigment. Pheomelanin synthesis may, therefore, be affected by cysteine homeostasis, although this has never been explored in a natural system. As diet is an important source of cysteine, here we indirectly tested for such an effect by searching for an association between food abundance and pheomelanin content of feathers in a wild population of Northern goshawk Accipiter gentilis. As predicted on the basis that CTNS expression may inhibit pheomelanin synthesis and increase with food abundance as previously found in other strictly carnivorous birds, we found that the feather pheomelanin content in nestling goshawks, but not in adults, decreased as the abundance of prey available to them increased. In contrast, variation in the feather content of the non-sulphurated melanin form (eumelanin) was only explained by sex in both nestlings and adults. We also found that the feather pheomelanin content of nestlings was negatively related to that of their mothers, suggesting a relevant environmental influence on pheomelanin synthesis. Overall, our findings suggest that variation in pheomelanin synthesis may be a side effect of the maintenance of cysteine homeostasis. This may help explaining variability in the expression of pigmented phenotypes.

Keywords

Animal pigmentation Cysteine homeostasis Melanogenesis Phenotypic plasticity Raptors 

Notes

Acknowledgements

We thank Rafael Palomo Santana for giving us permit to reproduce his goshawk photographs in Fig. 1. IG is supported by a Ramón y Cajal fellowship (RYC-2012–10237) and the project CGL2015-67796-P, both from the Spanish Ministry of Economy and Competitiveness (MINECO).

References

  1. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48CrossRefGoogle Scholar
  2. Burnham KP, Anderson DR (2002) Model selection and multimodel inference. A practical information-theoric approach. Springer-Verlag, New YorkGoogle Scholar
  3. Chiaverini C, Sillard L, Flori E et al (2012) Cystinosin is a melanosomal protein that regulates melanin synthesis. FASEB J 26:3779–3789CrossRefPubMedGoogle Scholar
  4. Core Team R (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  5. Fargallo JA, Laaksonen T, Korpimäki E, Wakamatsu K (2007) A melanin-based trait reflects environmental growth conditions of nestling male Eurasian kestrels. Evol Ecol 21:157–171CrossRefGoogle Scholar
  6. Fox J, Weisberg S (2011) An {R} Companion to Applied Regression, Second Edition. Sage, Thousand Oaks. URL: https://socserv.socsci.mcmaster.ca/jfox/Books/Companion
  7. Galván I (2017) Condition-dependence of pheomelanin-based coloration in nuthatches Sitta europaea suggests a detoxifying function: implications for the evolution of juvenile plumage patterns. Sci Rep 7:9138CrossRefPubMedPubMedCentralGoogle Scholar
  8. Galván I, Jorge A (2015) Dispersive Raman spectroscopy allows the identification and quantification of melanin types. Ecol Evol 5:1425–1431CrossRefPubMedPubMedCentralGoogle Scholar
  9. Galván I, Wakamatsu K (2016) Color measurement of the animal integument predicts the content of specific melanin forms. RSC Adv 6:79135–79142CrossRefGoogle Scholar
  10. 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 41:523–531CrossRefGoogle Scholar
  11. Galván I, Jorge A, Ito K, Tabuchi K, Solano F, Wakamatsu K (2013) Raman spectroscopy as a non-invasive technique for the quantification of melanins in feathers and hairs. Pigment Cell Melanoma Res 26:917–923CrossRefPubMedGoogle Scholar
  12. Galván I, Inácio Â, Nielsen ÓK (2017a) Gyrfalcons Falco rusticolus adjust CTNS expression to food abundance: a possible contribution to cysteine homeostasis. Oecologia 184:779–785CrossRefPubMedGoogle Scholar
  13. Galván I, Inácio Â, Romero-Haro AA, Alonso-Alvarez C (2017b) Adaptive downregulation of pheomelanin-related Slc7a11 gene expression by environmentally induced oxidative stress. Mol Ecol 26:849–858CrossRefPubMedGoogle Scholar
  14. García-Borrón JC, Olivares Sánchez MC (2011) Biosynthesis of melanins. In: Borovanský J, Riley PA (eds) Melanins and melanosomes: biosynthesis, biogenesis, physiological, and pathological functions. Wiley-Blackwell, Weinheim, pp 87–116CrossRefGoogle Scholar
  15. Giles NM, Watts AB, Giles GI, Fry FH, Littlechild JA, Jacob C (2003) Metal and redox modulation of cysteine protein function. Chem Biol 10:677–693CrossRefPubMedGoogle Scholar
  16. Heinsohn R, Legge S, Endler JA (2005) Extreme reversed sexual dichromatism in a bird without sex role reversal. Science 309:617–619CrossRefPubMedGoogle Scholar
  17. Hoy SR, Ball RE, Lambin X, Whitfield DP, Marquiss M (2015) Genetic markers validate using the natural phenotypic characteristics of shed feathers to identify individual northern goshawks Accipiter gentilis. J Avian Biol 47:43–47Google Scholar
  18. Hsu SL, Moore WH, Krimm S (1976) Vibrational spectrum of the unordered polypeptide chain: a Raman study of feather keratin. Biopolymers 15:1513–1528CrossRefPubMedGoogle Scholar
  19. Ito S, Nakanishi Y, Valenzuela 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 24:605–613CrossRefPubMedGoogle Scholar
  20. Johnsen A, Delhey K, Andersson S, Kempenaers B (2003) Plumage colour in nestling blue tits: sexual dichromatism, condition dependence and genetic effects. Proc R Soc Lond B 270:1263–1270CrossRefGoogle Scholar
  21. Kenward R (2006) The goshawk. Poyser, LondonGoogle Scholar
  22. Kim SY, Fargallo JA, Vergara P, Martínez-Padilla J (2013) Multivariate heredity of melanin-based coloration, body mass and immunity. Heredity 111:139–146CrossRefPubMedPubMedCentralGoogle Scholar
  23. Klasing KC (1998) Comparative avian nutrition. CAB International, WallingfordGoogle Scholar
  24. Kühlapfel O, Brune J (1995) Die Mauserfeder als Hilfsmittel zur Altersbestimmung und Individualerkennung von Habichten (Accipiter gentilis). Charadrius 31:120–125Google Scholar
  25. Lin BD, Mbarek H, Willemsen G et al (2015) Heritability and genome-wide association studies for hair color in a Dutch twin family based sample. Genes 6:559–576CrossRefPubMedPubMedCentralGoogle Scholar
  26. Møller AP, Nielsen JT (2007) Malaria and risk of predation: a comparative study of birds. Ecology 88:871–881CrossRefPubMedGoogle Scholar
  27. Møller AP, Nielsen JT (2014) Large increase in nest size linked to climate change: An indicator of life history, senescence and condition. Oecologia 179:913–921CrossRefGoogle Scholar
  28. Nielsen JT, Drachmann J (2003) Age-dependent reproductive performance in Northern Goshawks Accipiter gentilis. Ibis 145:1–8CrossRefGoogle Scholar
  29. Opdam P, Müskens G (1976) Use of shed feathers in population studies of Accipiter hawks (Aves, Accipitriformes, Accipitridae). Beaufortia 24:55–62Google Scholar
  30. Park S, Imlay JA (2003) High levels of intracellular cysteine promote oxidative DNA damage by driving the Fenton reaction. J Bacteriol 185:1942–1950CrossRefPubMedPubMedCentralGoogle Scholar
  31. Polidori C, Jorge A, Ornosa C (2017) Eumelanin and pheomelanin are predominant pigments in bumblebee (Apidae: Bombus) pubescence. PeerJ 5:e3300CrossRefPubMedPubMedCentralGoogle Scholar
  32. Roulin A, Dijkstra C (2003) Genetic and environmental components of variation in eumelanin and phaeomelanin sex-traits in the barn owl. Heredity 90:359–364CrossRefPubMedGoogle Scholar
  33. Saino N, Romano M, Rubolini D, Teplitsky C, Ambrosini R, Caprioli M, Canova L, Wakamatsu K (2013) Sexual dimorphism in melanin pigmentation, feather coloration and its heritability in the barn swallow (Hirundo rustica). PLoS ONE 8:e58024CrossRefPubMedPubMedCentralGoogle Scholar
  34. Stipanuk MH, Dominy JE Jr, Lee JI, Coloso RM (2006) Mammalian cysteine metabolism: new insights into regulation of cysteine metabolism. J Nutr 136:1652S–1659SCrossRefPubMedGoogle Scholar
  35. Stipanuk MH, Ueki I, Dominy JE Jr, Simmons CR, Hirschberger LL (2009) Cysteine dioxygenase: a robust system for regulation of cellular cysteine levels. Amino Acids 37:55–63CrossRefPubMedGoogle Scholar
  36. Vaanholt LM, De Jong B, Garland T Jr, Daan S, Visser GH (2007) Behavioural and physiological responses to increased foraging effort in male mice. J Exp Biol 210:2013–2024CrossRefPubMedGoogle Scholar
  37. Vaanholt LM, Speakman JR, Garland T Jr, Lobley GE, Visser GH (2008) Protein synthesis and antioxidant capacity in aging mice: e ects of long-term voluntary exercise. Physiol Biochem Zool 81:148–157CrossRefPubMedGoogle Scholar
  38. Viña J, Saez GT, Wiggins D, Roberts AFC, Hems R, Krebs HA (1983) The effect of cysteine oxidation on isolated hepatocytes. Biochem J 212:39–44CrossRefPubMedPubMedCentralGoogle Scholar
  39. Wang H, Osseiran S, Igras V et al (2016) In vivo coherent Raman imaging of the melanomagenesis-associated pigment pheomelanin. Sci Rep 6:37986CrossRefPubMedPubMedCentralGoogle Scholar
  40. Weimerskirch H, Ancel A, Caloin M, Zahariev A, Spagiari J, Kersten M, Chastel O (2003) Foraging efficiency and adjustment of energy expenditure in a pelagic seabird provisioning its chick. J Anim Ecol 72:500–508CrossRefGoogle Scholar
  41. Wente WH, Phillips JB (2003) Fixed green and brown color morphs and a novel color-changing morph of the Pacific tree frog Hyla regilla. Am Nat 162:461–473CrossRefPubMedGoogle Scholar
  42. Wu G, Fang YZ, Yang S, Lupton JR, Turner ND (2004) Glutathione metabolism and its implications for health. J Nutr 134:489–492CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Departamento de Ecología EvolutivaEstación Biológica de Doñana, CSICSevillaSpain
  2. 2.Laboratorio de Técnicas Analíticas No DestructivasMuseo Nacional de Ciencias Naturales, CSICMadridSpain
  3. 3.SindalDenmark
  4. 4.Ecologie Systématique EvolutionUniversité Paris-Sud, CNRS, AgroParisTech, Université Paris-SaclayOrsay CedexFrance

Personalised recommendations