Skip to main content
SpringerLink
Log in

Does body growth impair immune function in a large herbivore?

  • Physiological ecology - original research
  • Published:
Oecologia Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abbas F, Morellet N, Hewison AJM, Merlet J, Cargnelutti B, Lourtet B, Angibault JM, Daufresne T, Aulagnier S, Verheyden H (2011) Landscape fragmentation generates spatial variation of diet composition and quality in a generalist herbivore. Oecologia 167:401–411

    Article  Google Scholar 

  • Andersen R, Duncan P, Linnell JDC (1998) The European roe deer: the biology of success. Scandinavian University Press, Oslo

    Google Scholar 

  • Andersen R, Gaillard JM, Linnell JDC, Duncan P (2000) Factors affecting maternal care in an income breeder, the European roe deer. J Anim Ecol 69:672–682

    Article  Google Scholar 

  • Andersson MB (1994) Sexual Selection. Princeton University Press, Princeton

    Google Scholar 

  • Arendt JD, Wilson DS (1997) Optimistic growth: competition and an ontogenetic niche-shift select for rapid growth in pumpkinseed sunfish (Lepomis gibbosus). Evolution 51:1946–1954

    PubMed  Google Scholar 

  • Bartoń K (2016) MuMIn: multi-model inference. R package version 1.15.6. https://cran.r-project.org/web/packages/MuMIn/index.html

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

    Article  Google Scholar 

  • Bauch C, Becker PH, Verhulst S (2013) Telomere length reflects phenotypic quality and costs of reproduction in a long-lived seabird. Proc R Soc B 280:20122540

    Article  Google Scholar 

  • Beirne C, Delahay R, Young A (2015) Sex differences in senescence: the role of intra-sexual competition in early adulthood. Proc R Soc B 282:20151086

    Article  Google Scholar 

  • Blanckenhorn WU (2000) The evolution of body size: what keeps organisms small? Q Rev Biol 75:385–407

    Article  CAS  Google Scholar 

  • Bonenfant C, Gaillard JM, Coulson T, Festa-Bianchet M, Loison A, Garel M, Egil Loe L, Blanchard P, Pettorelli N, Owen-Smith N, Du Toit J, Duncan P (2009) Empirical evidence of density dependence in populations of large herbivores. Adv Ecol Res 41:314–345

    Google Scholar 

  • Brommer JE (2004) Immunocompetence and its costs during development: an experimental study in blue tit nestlings. Proc R Soc B 7:S110–S113

    Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New York

    Google Scholar 

  • Cheynel L, Lemaître JF, Gaillard JM, Rey B, Bourgoin G, Ferté H, Jégo M, Débias F, Pellerin M, Jacob L, Gilot-Fromont E (2017) Immunosenescence patterns differ between populations but not between sexes in a long-lived wild mammal. Sci Rep 7:13700

    Article  CAS  Google Scholar 

  • Civitello DJ, Cohen J, Fatima H, Halstead NT, Liriano J, McMahon TA, Ortega CN, Sauer EL, Sehgal T, Young S, Rohr JR (2015) Biodiversity inhibits parasites: broad evidence for the dilution effect. Proc Nat Acad Sci 112:8667–8671

    Article  CAS  Google Scholar 

  • Cody ML (1966) A general theory of clutch size. Evolution 20:174–184

    Article  Google Scholar 

  • Dmitriew CM (2011) The evolution of growth trajectories: what limits growth rate? Biol Rev 86:97–116

    Article  Google Scholar 

  • Douhard F, Gaillard JM, Pellerin M, Jacob L, Lemaître JF (2017) The cost of growing large: costs of post-weaning growth on body mass senescence in a wild mammal. Oikos 126:1329–1338

    Article  Google Scholar 

  • Dray S, Dufour AB (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22:1–20

    Article  Google Scholar 

  • Dupont-Prinet A, Chatain B, Grima L, Vandeputte M, Claireaux G, McKenzie DJ (2010) Physiological mechanisms underlying a trade-off between growth rate and tolerance of feed deprivation in the European sea bass (Dicentrarchus labrax). J Exp Biol 213:1143–1152

    Article  CAS  Google Scholar 

  • Gaillard JM, Yoccoz NG (2003) Temporal variation in survival of mammals: a case of environmental canalization? Ecology 84:3294–3306

    Article  Google Scholar 

  • Gaillard JM, Sempéré AJ, Boutin JM, Van Laere C, Boisaubert B (1992) Effects of age and body weight on the proportion of females breeding in a population of roe deer (Capreolus capreolus). Can J Zool 70:1541–1545

    Article  Google Scholar 

  • Gaillard JM, Delorme D, Boutin JM, Van Laere G, Boisaubert B, Pradel R (1993) Roe deer survival patterns—a comparative analysis of contrasting populations. J Anim Ecol 62:778–791

    Article  Google Scholar 

  • Gaillard JM, Delorme D, Boutin JM, Van Laere G, Boisaubert B (1996) Body mass of roe deer fawns during winter in 2 contrasting populations. J Wild Manag 60:29–36

    Article  Google Scholar 

  • Gaillard JM, Boutin JM, Delorme D, Van Laere G, Duncan P, Lebreton JD (1997) Early survival in roe deer: causes and consequences of cohort variation in two contrasted populations. Oecologia 112:502–513

    Article  Google Scholar 

  • Gaillard JM, Hewison AJ, Klein F, Plard F, Douhard M, Davison R, Bonenfant C (2013) How does climate change influence demographic processes of widespread species? Lessons from the comparative analysis of contrasted populations of roe deer. Ecol Lett 16:48–57

    Article  Google Scholar 

  • Garnier R, Cheung CK, Watt KA, Pilkington JG, Pemberton JM, Graham AL (2017) Joint associations of blood plasma proteins with overwinter survival of a large mammal. Ecol Lett 20:175–183

    Article  Google Scholar 

  • Geiger S, Le Vaillant M, Lebard T, Reichert S, Stier A, Le Maho Y, Criscuolo F (2012) Catching-up but telomere loss: half-opening the black box of growth and ageing trade-off in wild king penguin chicks. Mol Ecol 21:1500–1510

    Article  Google Scholar 

  • Gélin U, Wilson ME, Cripps J, Coulson G, Festa-Bianchet M (2015) Individual heterogeneity and offspring sex affect the growth–reproduction trade-off in a mammal with indeterminate growth. Oecologia 180:1127–1135

    Article  Google Scholar 

  • Gilot-Fromont E, Jégo M, Bonenfant C, Gibert P, Rannou B, Klein F, Gaillard JM (2012) Immune phenotype and body condition in roe deer: individuals with high body condition have different, not stronger immunity. PLoS One 7:e45576

    Article  CAS  Google Scholar 

  • Hanssen SA, Hasselquist D, Folstad I, Erikstad KE (2005) Cost of reproduction in a long-lived bird: incubation effort reduces immune function and future reproduction. Proc R Soc B 272:1039–1046

    Article  Google Scholar 

  • Hector KL, Nakagawa S (2012) Quantitative analysis of compensatory and catch-up growth in diverse taxa. J Anim Ecol 81:583–593

    Article  Google Scholar 

  • Hewison AJM, Vincent JP, Angibault JM, Delorme D, Van Laere G, Gaillard JM (1999) Tests of estimation of age from tooth wear on roe deer of known age: variation within and among populations. Can J Zool 77:58–67

    Article  Google Scholar 

  • Hewison AJM, Gaillard JM, Blanchard P, Festa-Bianchet M (2002) Maternal age is not a predominant determinant of progeny sex ratio variation in ungulates. Oikos 98:334–339

    Article  Google Scholar 

  • Hewison AJM, Morellet N, Verheyden H, Daufresne T, Angibault JM, Cargnelutti B, Merlet J, Picot D, Rames JL, Joachim J, Lourtet B, Serrano E, Bideau E (2009) Landscape fragmentation influences winter body mass of roe deer. Ecography 32:1062–1070

    Article  Google Scholar 

  • Hewison AJM, Gaillard JM, Delorme D, Van Laere G, Amblard T, Klein F (2011) Reproductive constraints, not environmental conditions, shape the ontogeny of sex-specific mass-size allometry in roe deer. Oikos 120:1217–1226

    Article  Google Scholar 

  • Hõrak P, Ots I, Tegelmann L, Møller AP (2000) Health impact of phytohaemagglutinin-induced immune challenge on great tit (Parus major) nestlings. Can J Zool 78:905–910

    Article  Google Scholar 

  • Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363

    Article  Google Scholar 

  • Houwen B (2001) The differential cell count. Lab Hematol 7:89–100

    Google Scholar 

  • Kirkwood TBL, Rose MR (1991) Evolution of senescence - late survival sacrificed for reproduction. Philos Trans R Soc B 332:15–24

    Article  CAS  Google Scholar 

  • Klasing KC (1998) Nutritional modulation of resistance to infectious diseases. Poultry Sci 77:1119–1125

    Article  CAS  Google Scholar 

  • Klasing KC (2004) The costs of immunity. Acta Zool Sin 50:961–969

    CAS  Google Scholar 

  • Lee KA (2006) Linking immune defenses and life history at the levels of the individual and the species. Int Comput Biol 46:1000–1015

    Article  CAS  Google Scholar 

  • Lee WS, Monaghan P, Metcalfe NB (2013) Experimental demonstration of the growth rate-lifespan trade-off. Proc R Soc B 280:20122370

    Article  Google Scholar 

  • Lemaître JF, Gaillard JM, Pemberton JM, Clutton-Brock TH, Nussey DH (2014) Early life expenditure in sexual competition is associated with increased reproductive senescence in male red deer. Proc R Soc B 281:20140792

    Article  Google Scholar 

  • Lemaître JF, Berger V, Bonenfant C, Douhard M, Gamelon M, Plard F, Gaillard JM (2015) Early-late life trade-offs and the evolution of ageing in the wild. Proc R Soc B 282:20150209

    Article  Google Scholar 

  • Lochmiller RL, Deerenberg C (2000) Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88:87–98

    Article  Google Scholar 

  • Lynsdale CL, Mumby HS, Hayward AD, Mar KU, Lummaa V (2017) Parasite-associated mortality in a long-lived mammal: variation with host age, sex, and reproduction. Ecol Evol 7:1–12

    Article  Google Scholar 

  • Matson KD, Robert E, Ricklefs RE, Klasing KC (2005) A hemolysis–hemagglutination assay for characterizing constitutive innate humoral immunity in wild and domestic birds. Dev Comput Immunol 29:275–286

    Article  CAS  Google Scholar 

  • Mauck RA, Matson KD, Philipsborn J, Ricklefs RE (2005) Increase in the constitutive innate humoral immune system in Leach’s Storm-Petrel (Oceanodroma leucorhoa) chicks is negatively correlated with growth rate. Funct Ecol 19:1001–1007

    Article  Google Scholar 

  • McDade TW (2005) Life history, maintenance, and the early origins of immune function. Am J Hum Biol 17:81–94

    Article  Google Scholar 

  • McDade TW, Georgiev AV, Kuzawa CW (2016) Trade-offs between acquired and innate immune defenses in humans. Evol Med Public Health 1:1–16

    Article  Google Scholar 

  • Metcalfe NB, Monaghan P (2001) Compensation for a bad start: grow now, pay later? Trends Ecol Evol 16:254–260

    Article  Google Scholar 

  • Metcalfe NB, Monaghan P (2003) Growth versus lifespan: perspectives from evolutionary ecology. Exp Gerontol 38:935–940

    Article  Google Scholar 

  • Morellet N, Verheyden H, Angibault JM, Cargnelutti B, Lourtet B, Hewison AJM (2009) The effect of capture on ranging behaviour and activity of the European roe deer Capreolus capreolus. Wildl Biol 15:278–287

    Article  Google Scholar 

  • Nakagawa S, Cuthill IC (2007) Effect size, confidence interval and statistical significance: a practical guide for biologists. Biol Rev Camb Philos Soc 82:591–605

    Article  Google Scholar 

  • Nakagawa S, Schielzeth H (2010) Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol Rev 85:935–956

    PubMed  Google Scholar 

  • Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2013) Package ‘vegan’. Community ecology package, version, vol 2(9)

  • Panagakis A, Hamel S, Côté SD (2017) Influence of early reproductive success on longevity and late reproductive success in an alpine ungulate. Am Nat 189:667–683

    Article  Google Scholar 

  • Pettorelli N, Gaillard JM, Mysterud A, Duncan P, Stenseth NC, Delorme D, Van Laere G, Toïgo C, Klein F (2006) Using a proxy of plant productivity (NDVI) to find key periods for animal performance: the case of roe deer. Oikos 112:565–572

    Article  Google Scholar 

  • Portier C, Duncan P, Gaillard JM, Guillon N, Sempéré AJ (2000) Growth of European roe deer: patterns and rates. Acta Theriol 45:87–94

    Article  Google Scholar 

  • R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Roff DA (1992) The evolution of life histories. Theory and analysis. Chapman and Hall, New York

    Google Scholar 

  • Roitt I, Brostoff J, Male D (1998) Immunology. Mosby, Maryland

    Google Scholar 

  • Ronget V, Gaillard JM, Coulson T, Garratt M, Gueyffier F, Lega JC, Lemaître JF (2018) Causes and consequences of variation in offspring body mass: meta-analyses in birds and mammals. Biol Rev. https://doi.org/10.1111/brv.12329

    Article  PubMed  Google Scholar 

  • Rossi S, Doucelin A, Le Potier M-F, Eraud C, Gilot-Fromont E (2013) Innate immunity correlates with host fitness in wild boar (Sus scrofa) exposed to classical swine fever. PLoS One 8:e79706

    Article  Google Scholar 

  • Saino N, Calza S, Møller AO (1998) Effects of a dipteran ectoparasite on immune response and growth trade-offs in barn swallow, Hirundo rustica, nestlings. Oikos 81:217–228

    Article  Google Scholar 

  • Sams MG, Lochmiller RL, Qualls C, Leslie DM, Payton ME (1996) Physiological correlates of neonatal mortality in an overpopulated herd of white-tailed deer. J Mammal 77:179–190

    Article  Google Scholar 

  • Sandland G, Minchella DJ (2003) Costs of immune defense: an enigma wrapped in an environmental cloak? Trends Parasitol 19:571–574

    Article  Google Scholar 

  • Schmid-Hempel P (2003) Variation in immune defence as a question of evolutionary ecology. Proc. R. Soc. B 270:357–366

    Article  Google Scholar 

  • Schneeberger K, Courtiol A, Czirják GÁ, Voigt CC (2014) Immune profile predicts survival and reflects senescence in a small, long-lived mammal, the greater sac-winged bat (Saccopteryx bilineata). PLoS One 9:e108268

    Article  Google Scholar 

  • Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol 11:317–321

    Article  CAS  Google Scholar 

  • Soler JJ, de Neve L, Pérez-Contreras T, Soler M, Sorci G (2003) Trade-off between immunocompetence and growth in magpies: an experimental study. Proc R Soc B 270:241–248

    Article  Google Scholar 

  • Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford

    Google Scholar 

  • Szàp T, Møller AP (1999) Cost of parasitism and host immune defence in the sand martin Riparia riparia: a role for parent–offspring conflict? Oecologia 119:9–15

    Article  Google Scholar 

  • Van der Most PJ, de Jong B, Parmentier HK, Verhulst S (2011) Trade-off between growth and immune function: a meta-analysis of selection experiments. Funct Ecol 25:74–80

    Article  Google Scholar 

  • Vanpé C, Gaillard JM, Morellet N, Kjellander P, Liberg O, Delorme D, Hewison AJM (2009) Age-specific variation in male breeding success of a territorial ungulate species, the European roe deer. J Mammal 90:661–665

    Article  Google Scholar 

  • Wieser W (1994) Cost of growth in cells and organisms: general rules and comparative aspects. Biol Rev Camb Philos Soc 69:1–33

    Article  CAS  Google Scholar 

  • Wilbourn RV, Froy H, McManus MC, Cheynel L, Gaillard JM, Gilot-Fromont E, Regis C, Rey B, Pellerin M, Lemaître JF, Nussey DH (2017) Age-dependent associations between telomere length and environmental conditions in roe deer. Biol Lett 13:20170434

    Article  Google Scholar 

  • Williams GC (1957) Pleiotropy, natural selection and the evolution of senescence. Evolution 11:398–411

    Article  Google Scholar 

  • Young H, Griffin RH, Wood CL, Nunn CL (2013) Does habitat disturbance increase infectious disease risk for primates? Ecol Lett 16:656–663

    Article  Google Scholar 

  • Zuk M, McKean KA (1996) Sex differences in parasite infections: patterns and processes. Int J Parasitol 26:1009–1023

    Article  CAS  Google Scholar 

  • Zuk M, Stoehr AM (2002) Immune defense and host life history. Am Nat 160:S9–S22

    Article  Google Scholar 

Download references

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 information

Authors and Affiliations

  1. Université de Lyon, Université Lyon 1, UMR CNRS 5558, Villeurbanne Cedex, France

    L. Cheynel, E. Gilot-Fromont, B. Rey, F. Débias, S. Pardonnet, J.-M. Gaillard & J.-F. Lemaître

  2. Université de Lyon, VetAgro Sup, Marcy-l’Etoile, France

    E. Gilot-Fromont

  3. CEFS, Université de Toulouse, INRA, Castanet Tolosan, France

    J. Carbillet, H. Verheyden & A. J. M. Hewison

  4. Office National de la Chasse et de la Faune Sauvage, Centre National de Recherches Appliquées sur les Cervidés-Sanglier, Bar-le-Duc, France

    M. Pellerin

  5. GenPhySE, Université de Toulouse, INRA, INPT, INP-ENVT, 31320, Castanet Tolosan, France

    F. Douhard

Authors
  1. L. Cheynel
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. F. Douhard
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. E. Gilot-Fromont
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. B. Rey
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. F. Débias
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. S. Pardonnet
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. J. Carbillet
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. H. Verheyden
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. A. J. M. Hewison
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. M. Pellerin
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. J.-M. Gaillard
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. J.-F. Lemaître
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

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.

Corresponding author

Correspondence to L. Cheynel.

Ethics declarations

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).

Additional information

Communicated by Jörg U. Ganzhorn.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cheynel, L., Douhard, F., Gilot-Fromont, E. et al. Does body growth impair immune function in a large herbivore?. Oecologia 189, 55–68 (2019). https://doi.org/10.1007/s00442-018-4310-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-018-4310-4

Keywords

Search

Navigation