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Unprecedented high catecholamine production causing hair pigmentation after urinary excretion in red deer

  • Ismael Galván
  • Francisco Solano
  • Mohammed Zougagh
  • Fernando de Andrés
  • Khaled Murtada
  • Ángel Ríos
  • Eva de la Peña
  • Juan Carranza
Original Article

Abstract

Hormones have not been found in concentrations of orders of magnitude higher than nanograms per milliliter. Here, we report urine concentrations of a catecholamine (norepinephrine) ranging from 0.05 to 0.5 g/l, and concentrations of its metabolite dl-3,4-dihydroxyphenyl glycol (DOPEG) ranging from 1.0 to 44.5 g/l, in wild male red deer Cervus elaphus hispanicus after LC–MS analyses. The dark ventral patch of male red deer, a recently described sexually selected signal, contains high amounts of DOPEG (0.9–266.9 mg/l) stuck in the hairs, while DOPEG is not present in non-darkened hair. The formation of this dark patch is explained by the chemical structure of DOPEG, which is a catecholamine-derived o-diphenol susceptible to be oxidized by air and form allomelanins, nitrogen-free pigments similar to cutaneous melanins; by its high concentration in urine; and by the urine spraying behavior of red deer by which urine is spread through the ventral body area. Accordingly, the size of the dark ventral patch was positively correlated with the concentration of DOPEG in urine, which was in turn correlated with DOPEG absorbed in ventral hair. These findings represent catecholamine concentrations about one million higher than those previously reported for any hormone in an organism. This may have favored the evolution of the dark ventral patch of red deer by transferring information on the fighting capacity to rivals and mates. Physiological limits for hormone production in animals are thus considerably higher than previously thought. These results also unveil a novel mechanism of pigmentation based on the self-application of urine over the fur.

Keywords

Allomelanins Catecholamines Deer Pigmentation Urine hormones 

Notes

Acknowledgements

Two anonymous reviewers made comments that improved the manuscript. Rafael Palomo Santana kindly allowed us to reproduce his red deer photographs, shown in Figs. 2 and 3. IG benefits from a Ramón y Cajal Fellowship (RYC-2012-10237) from Spain’s Ministry of Science, Innovation and Universities, and MZ benefits from an “INCRECYT” research contract. Financial support was obtained from projects CGL2013-48122-P, CGL2015-67796-P and CTQ2016-78793-P from Spain’s Ministry of Science, Innovation and Universities, and from project SBPLY/17/180501/000262 from Junta de Comunidades de Castilla-La Mancha.

Compliance with ethical standards

Ethical standards

All experiments were performed in compliance with the relevant laws and institutional guidelines in Spain.

Conflict of interest

The authors declare that they have no conflict of interest.

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Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Department of Evolutionary Ecology, Doñana Biological StationConsejo Superior de Investigaciones Científicas (CSIC)SevilleSpain
  2. 2.Department of Biochemistry and Molecular Biology B and Immunology, Faculty of MedicineUniversity of MurciaMurciaSpain
  3. 3.Regional Institute for Applied Scientific Research (IRICA)University of Castilla-La ManchaCiudad RealSpain
  4. 4.Department of Analytical Chemistry and Food Technology, Faculty of PharmacyUniversity of Castilla-La ManchaAlbaceteSpain
  5. 5.Department of Analytical Chemistry and Food Technology, Faculty of Chemical Science and TechnologyUniversity of Castilla-La ManchaCiudad RealSpain
  6. 6.Ungulate Research Unit, Cátedra de Recursos Cinegéticos y Piscícolas (CRCP)University of CordobaCórdobaSpain

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