Pheomelanin synthesis varies with protein food abundance in developing goshawks

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.

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References

  1. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48

    Article  Google Scholar 

  2. Burnham KP, Anderson DR (2002) Model selection and multimodel inference. A practical information-theoric approach. Springer-Verlag, New York

    Google Scholar 

  3. Chiaverini C, Sillard L, Flori E et al (2012) Cystinosin is a melanosomal protein that regulates melanin synthesis. FASEB J 26:3779–3789

    Article  CAS  PubMed  Google Scholar 

  4. Core Team R (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google 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 21:157–171

    Article  Google 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 7:9138

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Galván I, Jorge A (2015) Dispersive Raman spectroscopy allows the identification and quantification of melanin types. Ecol Evol 5:1425–1431

    Article  PubMed  PubMed Central  Google Scholar 

  9. Galván I, Wakamatsu K (2016) Color measurement of the animal integument predicts the content of specific melanin forms. RSC Adv 6:79135–79142

    Article  CAS  Google 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 41:523–531

    Article  Google 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 26:917–923

    Article  CAS  PubMed  Google 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 184:779–785

    Article  PubMed  Google 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 26:849–858

    Article  CAS  PubMed  Google 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 87–116

    Google 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 10:677–693

    Article  CAS  PubMed  Google Scholar 

  16. Heinsohn R, Legge S, Endler JA (2005) Extreme reversed sexual dichromatism in a bird without sex role reversal. Science 309:617–619

    Article  CAS  PubMed  Google 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 47:43–47

    Google Scholar 

  18. Hsu SL, Moore WH, Krimm S (1976) Vibrational spectrum of the unordered polypeptide chain: a Raman study of feather keratin. Biopolymers 15:1513–1528

    Article  CAS  PubMed  Google 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 24:605–613

    Article  CAS  PubMed  Google 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 270:1263–1270

    Article  Google Scholar 

  21. Kenward R (2006) The goshawk. Poyser, London

    Google Scholar 

  22. Kim SY, Fargallo JA, Vergara P, Martínez-Padilla J (2013) Multivariate heredity of melanin-based coloration, body mass and immunity. Heredity 111:139–146

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Klasing KC (1998) Comparative avian nutrition. CAB International, Wallingford

    Google Scholar 

  24. Kühlapfel O, Brune J (1995) Die Mauserfeder als Hilfsmittel zur Altersbestimmung und Individualerkennung von Habichten (Accipiter gentilis). Charadrius 31:120–125

    Google 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 6:559–576

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Møller AP, Nielsen JT (2007) Malaria and risk of predation: a comparative study of birds. Ecology 88:871–881

    Article  PubMed  Google 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 179:913–921

    Article  Google Scholar 

  28. Nielsen JT, Drachmann J (2003) Age-dependent reproductive performance in Northern Goshawks Accipiter gentilis. Ibis 145:1–8

    Article  Google Scholar 

  29. Opdam P, Müskens G (1976) Use of shed feathers in population studies of Accipiter hawks (Aves, Accipitriformes, Accipitridae). Beaufortia 24:55–62

    Google Scholar 

  30. Park S, Imlay JA (2003) High levels of intracellular cysteine promote oxidative DNA damage by driving the Fenton reaction. J Bacteriol 185:1942–1950

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Polidori C, Jorge A, Ornosa C (2017) Eumelanin and pheomelanin are predominant pigments in bumblebee (Apidae: Bombus) pubescence. PeerJ 5:e3300

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google 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:e58024

    Article  CAS  PubMed  PubMed Central  Google 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–1659S

    Article  CAS  PubMed  Google 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 37:55–63

    Article  CAS  PubMed  Google 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 210:2013–2024

    Article  PubMed  Google 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 81:148–157

    Article  CAS  PubMed  Google 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 212:39–44

    Article  PubMed  PubMed Central  Google Scholar 

  39. Wang H, Osseiran S, Igras V et al (2016) In vivo coherent Raman imaging of the melanomagenesis-associated pigment pheomelanin. Sci Rep 6:37986

    Article  CAS  PubMed  PubMed Central  Google 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 72:500–508

    Article  Google 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 162:461–473

    Article  PubMed  Google Scholar 

  42. Wu G, Fang YZ, Yang S, Lupton JR, Turner ND (2004) Glutathione metabolism and its implications for health. J Nutr 134:489–492

    Article  CAS  Google Scholar 

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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).

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Correspondence to Ismael Galván.

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Galván, I., Jorge, A., Nielsen, J.T. et al. Pheomelanin synthesis varies with protein food abundance in developing goshawks. J Comp Physiol B 189, 441–450 (2019). https://doi.org/10.1007/s00360-019-01222-y

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Keywords

  • Animal pigmentation
  • Cysteine homeostasis
  • Melanogenesis
  • Phenotypic plasticity
  • Raptors