Abstract

In animals, physiological mechanisms underlying reproductive and actuarial senescence remain poorly understood. Immunosenescence, the decline in the ability to display an efficient immune response with increasing age, is likely to influence both reproductive and actuarial senescence through increased risk of disease. Evidence for such a link has been reported from laboratory animal models but has been poorly investigated in the wild, where variation in resource acquisitions usually drives life-history trade-offs. We investigated immunosenescence patterns over 7 years in both sexes of two contrasting roe deer populations (Capreolus capreolus). We first measured twelve immune markers to obtain a thorough identification of innate and adaptive components of immunity and assessed, from the same individuals, the age-dependent variation observed in parasitic infections. Although the level of innate traits was maintained at old age, the functional innate immune traits declined with increasing age in one of two populations. In both populations, the production of inflammatory markers increased with advancing age. Finally, the adaptive response declined in late adulthood. The increasing parasite burden with age we reported suggests the effective existence of immunosenescence. Age-specific patterns differed between populations but not between sexes, which indicate that habitat quality could shape age-dependent immune phenotype in the wild.

Highlights

  • With increasing age, most organisms experience senescence, a process characterised by progressive and irreversible decline in age-specific reproductive success and survival[1]

  • The innate response mostly corresponds to the unspecific cellular response mediated principally by monocytes, natural killer and dendritic cells, while the adaptive response provides an antigen-specific response mediated by T and B lymphocytes

  • Inflammaging has multiple origins and may have many detrimental effects on organisms[25]. These age-related dysregulations and the subsequent reshaping of both components of the immune system can deeply affect the resistance against parasitism and infectious diseases of old individuals as suggested by the consistent increase in parasite burden with age reported so far

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Summary

Introduction

Most organisms experience senescence, a process characterised by progressive and irreversible decline in age-specific reproductive success (i.e. reproductive senescence) and survival (i.e. actuarial senescence)[1]. We aimed at investigating age-related changes of immune parameters and parasitic load, in males and females of two populations of roe deer Capreolus capreolus, subjected to highly different ecological contexts in the wild. In this weakly polygynous ungulate, both actuarial[36] and reproductive[37] senescence have been reported, as well as senescence in body mass[38], home range size[39] and haematological parameters[40]. Based on our current knowledge we predicted: (i) a progressive decline of the adaptive immune component but a stable innate response and an increased inflammatory markers in old individuals, (ii) an earlier and more pronounced immunosenescence in males than in females, (iii) an earlier and sharper immunosenescence in the population with poor and limited food resources (Chizé) than in the population with rich and abundant food resources (Trois-Fontaines), and (iv) an increase in parasitic load with age for individuals of a given sex in a given population

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