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

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.

野生动物在野外会承受显著的寄生虫压力，免疫防御对其生存至关重要。然而，由于脊椎动物免疫系统的复杂性，以及非模式生物（nonmodel organisms）中免疫试剂往往可用性有限，我们对于自然界中免疫功能与进化适合度之间的关联仍知之甚少。本研究借助兽医研究者为家养有蹄类（domestic ungulates）开发的方法与试剂，对野生索艾羊（Soay sheep）种群的血液样本开展检测，以评估一组覆盖范围异常广泛的免疫参数。本次检测涵盖了不同的先天免疫细胞与适应性免疫细胞类型，以及不同亚型的线虫特异性抗体。我们检验了这些标志物之间的相关性、它们随年龄组与性别的变化情况，尤为关键的是，它们能否预测不同人口统计群组内部或群组间的越冬存活率。我们发现，免疫标志物随年龄的变化模式符合预期，这与免疫发育过程相关；在剔除这些年龄趋势的影响后，我们检测的11种免疫标志物之间的相关性普遍较弱。我们发现，雌性个体的初始T细胞（naïve T cells）与γδ T细胞（gamma–delta T cells）比例显著高于雄性，且这一差异不受年龄影响；其余免疫标志物则未表现出性别差异。在11种标志物中，仅有一种能够预测越冬存活率：血浆中抗线虫IgG抗体水平更高的绵羊，在后续的高死亡率冬季中存活概率显著更高，且这一关联不受年龄、性别或体重的影响。这一结果印证了该研究体系此前基于另一组样本得出的发现，表明自然系统中针对生态相关寄生虫的循环抗体水平是免疫功能的一项重要参数，且可能处于强烈的自然选择压力之下。我们的数据罕见地揭示了野生种群中不同T细胞亚群与抗体水平随年龄组与性别群组的变异模式，并提示，某些类型的免疫反应——尤其是那些在个体内可重复、且与抗生态相关寄生虫抗性相关的免疫反应——或许最有助于研究自然条件下免疫与适合度之间的关联。