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

Abstract

Immune defenses are expected to be crucial for survival under the considerable parasite pressures experienced by wild animals. However, our understanding of the association between immunity and fitness in nature remains limited due to both the complexity of the vertebrate immune system and the often‐limited availability of immune reagents in nonmodel organisms. Here, we use methods and reagents developed by veterinary researchers for domestic ungulates on blood samples collected from a wild Soay sheep population, to evaluate an unusually broad panel of immune parameters. Our evaluation included different innate and acquired immune cell types as well as nematode parasite‐specific antibodies of different isotypes. We test how these markers correlate with one another, how they vary with age‐group and sex, and, crucially, whether they predict overwinter survival either within or among demographic groups. We found anticipated patterns of variation in markers with age, associated with immune development, and once these age trends were accounted for, correlations among our 11 immune markers were generally weak. We found that females had higher proportions of naïve T cells and gamma–delta T cells than males, independent of age, while our other markers did not differ between sexes. Only one of our 11 markers predicted overwinter survival: sheep with higher plasma levels of anti‐nematode IgG antibodies were significantly more likely to survive the subsequent high mortality winter, independent of age, sex, or weight. This supports a previous finding from this study system using a different set of samples and shows that circulating antibody levels against ecologically relevant parasites in natural systems represent an important parameter of immune function and may be under strong natural selection. Our data provide rare insights into patterns of variation among age‐ and sex groups in different T‐cell subsets and antibody levels in the wild, and suggest that certain types of immune response—notably those likely to be repeatable within individuals and linked to resistance to ecologically relevant parasites—may be most informative for research into the links between immunity and fitness under natural conditions.

Survival costs of reproduction are mediated by parasite infection in wild Soay sheep

“…We found the effects of sex and/or reproductive allocation on spring FEC became more apparent in adults compared to juveniles and yearlings: juvenile FEC was not influenced by sex or reproductive status; there was marginal evidence that yearling FEC was influenced by sex; and adult FEC was influenced by both. Juveniles had generally high FEC, as predicted from previous research on other wild vertebrates (Wilson et al 1996;Isomursu et al 2006;Hayward 2013;Watson et al 2016) and humans (Simon et al 2015), which suggests that juveniles have not developed fully effective immune defences. Yearling males tended to have higher spring FEC than females (marginal statistical support; estimate = 0.36 AE 0.17 SE, DAIC = À1; evidence ratio = 0.63); this result is consistent with studies from diverse species that have found males to have less effective immune responses (Tschirren et al 2003;Hayward 2013;Klein & Flanagan 2016;Watson et al 2016).…”

“…; Hayward ; Watson et al . ) and humans (Simon et al . ), which suggests that juveniles have not developed fully effective immune defences.…”

“…; Watson et al . ), and the re‐emergence of larvae from arrested development in spring (Langrová et al . ).…”

Reproductive effort influences intra‐seasonal variation in parasite‐specific antibody responses in wild Soay sheep

“…Previous analyses have revealed strong positive associations between different antibody isotypes measured in Soay sheep plasma (Nussey et al, ; Watson et al, ) and faeces (Watt et al, ) and have shown that T. circumcincta ‐specific pan‐isotypic antibody contains substantial among‐individual variation (Hayward et al, ). We aimed to build upon this work by estimating the individual‐level variation (repeatability) and individual‐level correlations between antibody measures with multivariate mixed‐effects models in ASReml‐R ver 3.0 (Gilmour, Gogel, Cullis, & Thompson, ) with the dataset of 248 samples from 54 females.…”

Parasite infections in a social carnivore: Evidence of their fitness consequences and factors modulating infection load

“…In mammals, age is one intrinsic factor that can alter resistance to infection, because immune processes generally improve from early life to adulthood and then decline in old age (Simon, Hollander, & McMichael, 2015). When young, the cellular immune responses of juveniles typically differ both qualitatively and quantitatively from those of adults (Ramsburg, Tigelaar, Craft, & Hayday, 2003;Watson et al, 2016) and juveniles are less likely to have the acquired immunity that develops following exposure to pathogen antigen than adults, (Cattadori, Boag, Bjørnstad, Cornell, & Hudson, 2005;Ferreira, Torelli, et al, 2019), and thus, juveniles are generally more vulnerable to infection than adults.…”