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Stress response varies with plumage colour and local habitat in feral pigeons

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Abstract

Bird populations exposed to different extrinsic conditions often differ in the responsiveness of the hypothalamo–pituitary–adrenal (HPA) axis and thus in corticosterone response that individuals mount when facing stressful events. However, the contribution of genetic variation to among-individual variability in HPA axis responsiveness across different environmental conditions is poorly understood. Melanin-based coloured types provide reliable phenotypic markers of alternative genotypes underlying stress coping styles. Large variations in melanin-based colouration are heritable in feral pigeons. We tested whether melanin-based colouration is associated with variation in corticosterone stress response in feral pigeons. To this end, we examined how corticosterone response varies both within and between differently coloured individuals across different environmental conditions. Differently coloured individuals produced different stress-induced corticosterone levels in relation to their environmental conditions: dark pigeons exhibited a higher corticosterone when originating from rural habitats, while this was not observed in pale pigeons. This suggests that among-population variation in stress response is higher in dark pigeons, this variation possibly reflecting adjustment and/or (epi)genetic adaptation to environmental conditions. In addition, corticosterone response increased with the degree of melanin-based colouration in pigeons originating from rural habitats but not in pigeons originating from more urbanized populations, resulting in the coexistence of alternative stress responses in some populations, but not in others. Our results suggest that species with melanin-based variation in differently urbanized populations along rural–urban gradients are potentially good candidate systems for studying stress coping styles under alternative selective regimes.

Zusammenfassung

Die Reaktion auf Stress variiert bei Straßentauben in Abhängigkeit von Gefiederfärbung und dem lokalen Lebensraum Vogelpopulationen, die verschiedenen Umweltbedingungen ausgesetzt sind, unterscheiden sich häufig in den Reaktionen der Hypothalamus-Hypophysen-Nebennierenrinden-Achse (HPA-Achse = hypothalamo-pitituary-adrenal axis) und somit in der Corticosteronantwort, die Individuen zeigen, wenn sie mit Stresssituationen konfrontiert werden. Allerdings ist noch wenig über den Beitrag der genetischen Variation zur Variabilität der HPA-Achsen-Reaktion zwischen Individuen unter verschiedenen Umweltbedingungen bekannt. Melaninbasierte Färbungstypen liefern verlässliche phänotypische Marker für die alternativen Genotypen, die Stressbewältigungsarten zugrunde liegen. Starke Variationen in der melaninbasierten Färbung sind bei Straßentauben Columba livia f. dom. erblich bedingt. Wir prüften, ob die melaninbasierte Färbung bei Straßentauben mit Unterschieden in der Corticosteron-Stressreaktion zusammenhängt. Dazu untersuchten wir, inwiefern die Corticosteronantwort unter verschiedenen Umweltbedingungen sowohl bei gleichartig als auch zwischen verschieden gefärbten Individuen variiert. Unterschiedlich gefärbte Individuen erreichten in Abhängigkeit von den Umweltbedingungen verschiedene stressinduzierte Corticosteronwerte: Dunkle Tauben zeigten höhere Corticosteronwerte, wenn sie aus ländlichen Habitaten stammten, während ein solcher Zusammenhang bei hellen Tauben nicht beobachtet werden konnte. Dies legt nahe, dass die Variation in der Stressreaktion zwischen Populationen bei dunklen Tauben größer ist, was möglicherweise eine Angleichung und/oder (epi-)genetische Anpassung an die Umweltbedingungen wiederspiegelt. Weiterhin stieg die Corticosteronantwort bei Tauben aus dem ländlichen Umfeld mit dem Grad der melaninbasierten Färbung an, nicht jedoch bei den Tauben aus den stärker verstädterten Populationen, was zum Nebeneinanderbestehen alternativer Stressreaktionstypen in manchen Population führt, in anderen dagegen nicht. Unsere Ergebnisse deuten an, dass Arten mit melaninbasierter Variation in unterschiedlich stark verstädterten Populationen entlang eines Stadt-Land-Gradienten potenziell geeignete Kandidatensysteme für Studien zu Stressbewältigungsstrategien unter verschiedenen Selektionsbedingungen bieten.

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Acknowledgments

We thank Thomas Charachon from the Mairie de Paris and Adeline Loyau from the Ferme Traditionnelle Educative de Mandres-Les-Roses for logistic support during the captures. We are grateful to the CEREEP station, Philippe Lenouvel and Aurélien Mouton for great help at different stages of this study. This work was supported by a grant from the Centre National de la Recherche Scientifique and from Université Pierre et Marie Curie. The experiments comply with the current French laws. All experiments were conducted under the authorization of the Direction Départementale des Services Vétérinaires de Seine-et-Marne (Authorization No. 77-07).

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Authors and Affiliations

  1. Sorbonne Universités, UPMC Univ Paris 06, UPEC, Paris 7, CNRS, INRA, IRD, Institut d’Ecologie et des Sciences de l’Environnement de Paris, 75005, Paris, France

    Hélène Corbel, Ariane Legros, Claudy Haussy, Lisa Jacquin, Julien Gasparini, Battle Karimi & Adrien Frantz

  2. Univ. Toulouse 3 Paul Sabatier, CNRS, ENFA, UMR 5174 EDB (Laboratoire Evolution and Diversité Biologique), 31062, Toulouse, France

    Lisa Jacquin

  3. Institute of Ecology and Environmental Sciences, Paris, 7, quai Saint-Bernard, Bât. A 7ème étage (Case 237), 75252, Paris Cedex 05, France

    Adrien Frantz

Authors
  1. Hélène Corbel
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  2. Ariane Legros
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  3. Claudy Haussy
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  4. Lisa Jacquin
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  5. Julien Gasparini
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  6. Battle Karimi
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  7. Adrien Frantz
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Corresponding author

Correspondence to Adrien Frantz.

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Conflict of interest

The authors declare that they have no conflict of interest.

All applicable international, national and/or institutional guidelines for the care and use of animals were followed.

This article does not contain any studies with human participants performed by any of the authors.

Informed consent was obtained from all individual participants included in the study.

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Communicated by L. Fusani.

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Corbel, H., Legros, A., Haussy, C. et al. Stress response varies with plumage colour and local habitat in feral pigeons. J Ornithol 157, 825–837 (2016). https://doi.org/10.1007/s10336-016-1331-9

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  • DOI: https://doi.org/10.1007/s10336-016-1331-9

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