An infectious personality: immune personalities and their role in the transmission of wildlife infectious diseases

免疫功能是动物最易变的特征之一，在个体之间和种群之间存在显著差异。然而，人们越来越认识到，在动物种群中，随着时间的推移，许多个体经历了可预测的和相对稳定的免疫反应。在个体间高度变异的背景下，这种个体内的稳定性导致了某些免疫特征的中高重复性，术语“免疫个性”被用来描述随着时间和跨环境的这些一致的反应。自由放养动物种群中这些免疫个性的起源尚不清楚，但最近来自实验室动物和人类种群的证据表明，免疫表型的大部分多样性是由于生命早期接触环境病原体和微生物共生体(微生物群)造成的。这些生命早期的微生物暴露可以直接刺激不同的免疫途径，在免疫系统中留下长期的印记，有时还会在免疫特征中产生更高水平的个体内差异。有趣的是，在人体中的初步研究表明，随着时间的推移，更多的可变免疫反应预示着对疫苗接种的更好反应。同样，我们最近在野生动物种群中发现，具有较低个体内差异水平的免疫个性会增加结核病感染的风险。因此，野生动物在生命早期暴露于不同的病原体和微生物群中，可能会形成独特的免疫个性，从而增加它们传播传染病的机会。为了验证这一假设，在这个研究项目中，我们将使用一种独特的寄主寄生虫系统(南美毛海豹和钩虫[Uncinaria sp.])这使得早期接触病原体和共生体的操作变得容易，并允许对免疫个性和自然获得性感染进行纵向跟踪。利用这个模型，我们将：i)表征新生儿钩虫感染对宿主微生物群的影响，以及ii)测试这种早期生命中受干扰的微生物群对成人免疫个性的影响。同时，我们将评估这些不同的免疫个性对流感病毒和海豹结核病(羽状分枝杆菌)感染风险和脱落模式的影响。这项研究计划将揭示野生动物系统中免疫个性的最重要驱动因素，并将确定这些个性对重要传染病传播的影响程度。更好地了解自由放养动物种群中免疫个性的驱动因素和后果，对于通过环境监测确定感染风险较高的个人和种群至关重要。该计划还将提供更好的工具来预测环境变化对野生动物免疫的影响和重要传染病的出现。

Immune function is one of the most variable traits in animals with significant differences between individuals and between populations. However, it is increasingly recognized that in animal populations many individuals experience predictable and relatively stable immune responses over time. This within-individual stability in a context of high between-individual variance leads to intermediate to high repeatability in some immune traits, and the term "immune personality" has been used to describe these consistent responses over time and across environments. The origin of these immune personalities in free-ranging animal populations is not clear but recent evidence from lab animal and human populations suggests that most of the diversity in immune phenotypes is due to early life exposure to environmental pathogens and microbial commensals (microbiome). These early life microbial exposures can directly stimulate different immune pathways leaving a long-lasting imprinting in the immune system and sometimes higher levels of within-individual variance in immune traits. Interestingly, preliminary studies in people suggest that more variable immune responses overtime predict better response to vaccination. Similarly, we recently found in a wild animal population that immune personalities characterized by lower levels of within-individual variance increase tuberculosis infection risk. Therefore, wild animals exposed to different pathogens and microbiomes during early life could develop unique immune personalities that increase their chances to disseminate infectious diseases. To test this hypothesis, in this research program we will use a unique host parasite system (South American fur seal and hookworm [Uncinaria sp.]) that allows for easy manipulation of early life exposure to pathogens and commensals and allows for longitudinal tracking of immune personalities and naturally acquired infections. Using this model, we will: i) characterize the effects of neonatal hookworm infection on the host microbiome, and ii) test the effects of this disturbed microbiomes during early life on the adult immune personality. Simultaneously, we will assess the impact of these different immune personalities on the infection risk and shedding patterns of influenza viruses and seal tuberculosis (Mycobacterium pinnipediae). This research program will reveal the most important drivers of immune personalities in wildlife systems and will determine the extent of the effects of these personalities on the transmission of important infectious diseases. A better understanding on the drivers and consequences of immune personalities in free-ranging animal populations will be critical to identify through environmental monitoring individuals and populations at higher risk of infection. This program will also offer better tools to predict the impact of environmental change on wildlife immunity and the emergence of important infectious diseases