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Oecologia

, Volume 189, Issue 1, pp 55–68 | Cite as

Does body growth impair immune function in a large herbivore?

  • L. CheynelEmail author
  • F. Douhard
  • E. Gilot-Fromont
  • B. Rey
  • F. Débias
  • S. Pardonnet
  • J. Carbillet
  • H. Verheyden
  • A. J. M. Hewison
  • M. Pellerin
  • J.-M. Gaillard
  • J.-F. Lemaître
Physiological ecology - original research

Abstract

According to the principle of allocation, trade-offs are inevitable when resources allocated to one biological function are no longer available for other functions. Growth, and to a lesser extent, immunity are energetically costly functions that may compete with allocation to reproductive success and survival. However, whether high allocation to growth impairs immune system development during the growing period or immune system performance during adulthood is currently unknown in wild mammals. Using three roe deer (Capreolus capreolus) populations experiencing contrasting environmental conditions, we tested for potential costs of growth on immune phenotype over both the short-term (during growth), and the long-term (during adulthood) over the course of an individuals’ life. We investigated potential costs on a set of 12 immune traits that reflect both innate and adaptive responses, and compared them between sexes and populations. Although fast growth tended to be associated with low levels of some humoral traits (globulins) during the growing period and some cellular immune traits (i.e. eosinophil and neutrophil counts) during adulthood, evidence for a trade-off between growth and other immune components was limited. Unexpectedly, no detectable growth costs on immunity were found in females from the population experiencing the least favourable environment. We discuss our findings in the light of the complex interplay between resource allocation strategies among reproduction, maintenance and immunity, in relation to local environmental conditions experienced by roe deer.

Keywords

Body mass Eco-immunology Life history Roe deer Trade-off 

Notes

Acknowledgements

We thank all the ONCFS staff, in particular Claude Warnant and Gilles Capron, the local hunting associations, the Fédération Départementale des Chasseurs de la Haute Garonne and the field volunteers for the organisation of the roe deer captures. We thank Corinne Régis, Marie-Thérèse Poirel, Slimania Benabed, Damien Jouet and Elodie Moissonier for their help in the laboratory analyses and Anne-Béatrice Dufour for statistical advices. We also warmly thank two anonymous referees whose insightful comments substantially improved the manuscript. This work was supported by grants from the Agence Nationale de la Recherche (ANR-15-CE32-0002-01) and the ONCFS (Grants 2011/18/6171 and 2015/19/6171), and performed within the framework of the LABEX ECOFECT (ANR-11-LABX-0048) of Université de Lyon, within the program “Investissementsd’Avenir” (ANR-11-IDEX-0007) operated by the French National Research Agency (ANR).

Author contribution statement

JFL, JMG, EGF conceived the study and designed methodology; all authors collected the data; LC, EGF, BR, HV performed the immunological measures; LC and FD analysed the data; LC wrote the first draft of the paper and all authors contributed critically to the drafts and gave approval for the final version.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable institutional and/or national guidelines for the care and use of animals were followed. For Trois-Fontaines and Chizé populations, the protocol of capture and blood sampling of roe deer under the authority of the Office National de la Chasse et de la Faune Sauvage (ONCFS) was approved by the Director of Food, Agriculture and Forest (Prefectoral order 2009-14 from Paris). All procedures were approved by the Ethical Committee of Lyon 1 University (project DR2014-09, June 5, 2014). For the Aurignac population, the study was permitted by the land manager of both sites, the Office National des Forêts (ONF) and prefecture of Haute Garonne (Partnership Convention ONCFS-ONF dated 2005-12-23). All procedures were approved by the Ethical Committee 115 of Toulouse (project APAFIS#7880-2016120209523619v5).

Supplementary material

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Supplementary material 1 (DOCX 681 kb)
442_2018_4310_MOESM2_ESM.docx (492 kb)
Supplementary material 2 (DOCX 491 kb)
442_2018_4310_MOESM3_ESM.docx (34 kb)
Supplementary material 3 (DOCX 34 kb)
442_2018_4310_MOESM4_ESM.docx (24 kb)
Supplementary material 4 (DOCX 23 kb)

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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • L. Cheynel
    • 1
    Email author
  • F. Douhard
    • 5
  • E. Gilot-Fromont
    • 1
    • 2
  • B. Rey
    • 1
  • F. Débias
    • 1
  • S. Pardonnet
    • 1
  • J. Carbillet
    • 3
  • H. Verheyden
    • 3
  • A. J. M. Hewison
    • 3
  • M. Pellerin
    • 4
  • J.-M. Gaillard
    • 1
  • J.-F. Lemaître
    • 1
  1. 1.Université de Lyon, Université Lyon 1, UMR CNRS 5558Villeurbanne CedexFrance
  2. 2.Université de Lyon, VetAgro SupMarcy-l’EtoileFrance
  3. 3.CEFS, Université de Toulouse, INRACastanet TolosanFrance
  4. 4.Office National de la Chasse et de la Faune SauvageCentre National de Recherches Appliquées sur les Cervidés-SanglierBar-le-DucFrance
  5. 5.GenPhySE, Université de Toulouse, INRA, INPT, INP-ENVTCastanet TolosanFrance

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