Haematological parameters do senesce in the wild: evidence from different populations of a long‐lived mammal

Abstract

Increasing evidence of senescence has been reported from long-term studies of wild populations. However, most studies have focused on life-history traits like survival, reproduction or body mass, generally from a single intensively monitored population. However, variation in the intensity of senescence across populations, and to a lesser extent between sexes, is still poorly understood. In addition, the pattern of age-specific changes in haematological parameters remains virtually unknown to date for any population of vertebrate living in the wild. Using repeated blood samples collected from known-aged (2-15 years of age) roe deer (Capreolus capreolus) from two populations facing highly different environmental conditions, we filled the gap. In particular, we investigated age-specific changes in haematocrit, albumin and creatinine. We reported clear evidence of senescence in all haematological parameters. Moreover, senescence patterns differed between sexes and populations. The rate of senescence was higher in males than in females for haematocrit with no site difference. On the other hand, the rate of senescence in creatinine was higher at Trois Fontaines than at Chiz e with no sex difference. Our findings provide a first demonstration of age-specific declines in haematological parameters in wild populations of large herbivores and show that the process of senescence in vertebrates is not restricted to body mass or fitness components. We also demonstrate that the senescence pattern of haematological parameters is context dependent and varies both between sexes and according to environmental conditions.

The Williams' legacy: A critical reappraisal of his nine predictions about the evolution of senescence

“… for body mass, and Jégo et al. for hematocrit and creatinine). The intercept of each age‐dependent function has been selected to display differences in onsets of senescence across traits and has no biological meaning.…”

Sex‐independent senescence in a cooperatively breeding mammal

“…In addition, most studies of sex differences in senescence have focussed on mortality data , but to understand the mechanisms underlying age-related changes in fitness in naturally regulated populations, it is important to examine age-related changes in other biological parameters that are associated with individual performance and indicate why the sexes differ. This might include age-specific changes in reproductive effort , body mass and condition (Hämäläinen et al, 2014;Tafani et al, 2013), immune function (Beirne, Waring, McDonald, Delahay, & Young, 2016), and haematological parameters (Jégo et al, 2014), amongst others (Nussey, Froy, Lemaître, Gaillard, & Austad, 2013). From such work, it has become increasingly clear that different fitness-related traits can display divergent age-related trajectories within individuals (Evans, Gustafsson, & Sheldon, 2011;Hayward et al, 2015;Nussey et al, 2009), and are not necessarily closely related to each other (Bouwhuis, Choquet, Sheldon, & Verhulst, 2012 and highlight the need to consider a wider range of life histories to better understand the operation of senescence in natural populations.…”

Cellular and humoral immunity in a wild mammal: Variation with age & sex and association with overwinter survival

“…Variation in markers associated with immune function with age has been widely reported in wild vertebrates (Cichoń, Sendecka, & Gustafsson, 2003; Jego et al., 2014; Nussey, Watt, Pilkington, Zamoyska, & McNeilly, 2012; Palacios, Winkler, Klasing, Hasselquist, & Vleck, 2011). Notably, the structure and function of the thymus in mammals and in birds deteriorates remarkably early in life in many vertebrates and the output of naïve T cells may be greatly reduced by the time an individual reaches sexual maturity (Cockburn, 1992; Møller & Erritzøe, 2001).…”

“…Profound changes in immune phenotype and function are observed over the course of an organism's lifespan, with resistance to infection typically developing through early life into adulthood and certain aspects of immune function becoming compromised in old age (Simon, Hollander, & McMichael, 2015). Variation in markers associated with immune function with age has been widely reported in wild vertebrates (Cichoń, Sendecka, & Gustafsson, 2003;Jego et al, 2014;Nussey, Watt, Pilkington, Zamoyska, & McNeilly, 2012;Palacios, Winkler, Klasing, Hasselquist, & Vleck, 2011). Notably, the structure and function of the thymus in mammals and in birds deteriorates remarkably early in life in many vertebrates and the output of naïve T cells may be greatly reduced by the time an individual reaches sexual maturity (Cockburn, 1992;Møller & Erritzøe, 2001).…”