Age‐related variation in immunity in a wild mammal population

Abstract

SummaryAge-related changes in immunity are well documented in humans and laboratory mammals. Using blood samples collected from wild Soay sheep, we show that pronounced differences in T-cell subsets and inflammatory markers amongst age classes are also evident under natural conditions. These shifts parallel those observed in mammals experiencing protected environments. We found progressive declines in the proportion of naïve CD4 T cells with age, a precipitous drop in γδ T cells after the second year of life and an increase in acute phase protein levels amongst geriatric sheep. Our findings suggest immune aging patterns observed in laboratory and domestic mammals may generalize to more complex, challenging environments and could have fitness costs under natural conditions.

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

“…Lymphocytes were preserved in fixative after collection on St Kilda and later analyzed, following antibody labeling, by flow cytometry in Edinburgh (following Nussey et al., 2012). Briefly, red cells were removed from 1 ml of whole blood by addition of 5 ml of ammonium chloride lysing solution (1.5 mol/L NH4Cl, 100 mmol/L NAHCO3, 10 mmol/L Na2EDTA), which was added to 1 ml of whole blood and mixed gently before centrifuging at 1008 g for 10 min.…”

“…(2012) with some modifications as described in full in the Supplementary Methods file. Fluorescently labeled monoclonal antibodies were used to identify the proportions of T helper cells (CD4+), cytotoxic T cells (CD8+), and gamma–delta T cells (γδ TcR+) within the total lymphocyte population within each sample and the proportion of T helper cells which were Treg (FoxP3+).…”

“…A small number of extreme outliers were identified in the raw data, and because these lay outside what seemed a biologically plausible range based on previous studies (Egbe‐Nwiyi, Nwaosu, & Salami, 2000; Holman, 1944; Nussey et al., 2012; Pisek, Travnicek, Salat, Kroupova, & Soch, 2008), we excluded them from further analyses. This included 2 data points for NLR (both >6), 2 for eosinophil counts (>30%), 2 for CD8+ (>25% of lymphocytes), and one for CD4+FoxP3+ (>65% of CD4+ T cells).…”

“…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).…”

“…Our work builds on a previous study which documented patterns of age‐related change in T‐cell subtypes consistent with those observed in the human, laboratory rodent, and domestic ruminant literature, but had insufficient sample sizes to meaningfully test for associations with fitness measures independently of age (Nussey et al., 2012). We have also previously shown that antibodies against a highly prevalent gastrointestinal nematode parasite in our study population, Teladorsagia circumcincta (Tc), are negatively associated with parasite egg counts and positively associated with overwinter survival in adult Soay sheep (Coltman, Wilson, Pilkington, Stear, & Pemberton, 2001; Hayward et al., 2014; Nussey et al., 2014).…”