Watson Rebecca L, McNeilly Tom N, Watt Kathryn A, Pemberton Josephine M, Pilkington Jill G, Waterfall Martin, Hopper Phoebe R T, Cooney Daniel, Zamoyska Rose, Nussey Daniel H
School of Biological Sciences Institutes of Evolutionary Biology & Immunology and Infection Research University of Edinburgh Edinburgh UK.
Moredun Research Institute Midlothian UK.
Ecol Evol. 2016 Nov 15;6(24):8695-8705. doi: 10.1002/ece3.2584. eCollection 2016 Dec.
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.
在野生动物面临的巨大寄生虫压力下，免疫防御对于生存至关重要。然而，由于脊椎动物免疫系统的复杂性以及非模式生物中免疫试剂通常有限，我们对自然界中免疫力与健康状况之间关联的理解仍然有限。在这里，我们使用兽医研究人员为家养有蹄类动物开发的方法和试剂，对从野生索艾羊种群采集的血样进行检测，以评估一组异常广泛的免疫参数。我们的评估包括不同的先天性和获得性免疫细胞类型以及不同亚型的线虫寄生虫特异性抗体。我们测试了这些标志物之间的相互关系、它们如何随年龄组和性别变化，以及至关重要的是，它们是否能预测不同人口统计学群体内部或之间的越冬存活率。我们发现，与免疫发育相关的标志物随年龄呈现出预期的变化模式，一旦考虑到这些年龄趋势，我们的11种免疫标志物之间的相关性通常较弱。我们发现，雌性幼稚T细胞和γδT细胞的比例高于雄性，且与年龄无关，而我们的其他标志物在性别之间没有差异。我们的11种标志物中只有一种能预测越冬存活率：抗线虫IgG抗体血浆水平较高的绵羊在随后的高死亡率冬季存活的可能性显著更高，且与年龄、性别或体重无关。这支持了此前在该研究系统中使用不同样本集得出的一项发现，并表明自然系统中针对生态相关寄生虫的循环抗体水平代表了免疫功能的一个重要参数，可能受到强烈的自然选择。我们的数据为野生环境中不同年龄组和性别组在不同T细胞亚群和抗体水平上的变化模式提供了难得的见解，并表明某些类型的免疫反应——尤其是那些可能在个体内部具有可重复性且与对生态相关寄生虫的抗性相关的反应——对于研究自然条件下免疫力与健康状况之间的联系可能最具参考价值。
