BEE NSFDEB-NERC: The eco-evolutionary dynamics of age-specific resistance to infectious disease

当一种流行病席卷植物、动物或人类的种群时，种群中最年轻的个体往往受到的打击最大。这是因为青少年通常比成年人更容易感染传染病。事实上，麻疹和水痘等许多人类疾病的传播主要是由儿童引起的。同样，在许多野生动物物种中，新的高度易感幼崽的春季“脉搏”可能引发流行病，包括有可能蔓延到人类或牲畜种群的疾病。然而，我们对为什么青少年天生如此易感缺乏基本的了解，即使在考虑了先前的疾病暴露之后也是如此。本研究将利用数学模型和模式植物系统的实验来研究驱动年龄特异性易感性进化的基本生态和进化过程。该结果将大大增加我们对抗性进化与疾病传播之间反馈的理解，这将改善野生动物疾病的管理策略，并为作物抗病育种提供信息。该研究还将通过与基础研究相结合的新的公民科学推广活动，增加公众对科学的了解，丰富当地生物多样性记录和博物馆收藏。从进化的角度来看，为什么幼体如此容易感染疾病的问题令人困惑，因为在繁殖之前感染似乎比在生命后期（宿主有机会繁殖之后）感染对宿主的负面影响要大得多。因此，自然选择应该倾向于那些年轻时不易患病的个体。该项目将验证一个新的假设，即幼体的易感性是通过宿主抗性的进化变化和疾病丰度的生态变化之间的反馈来维持的。这些“生态进化”反馈之所以发生，是因为宿主种群在任何年龄阶段的抗病进化反过来可以降低疾病流行的强度。至关重要的是，较低的疾病水平使寄主不太可能在幼年时遇到疾病，从而使幼年易感性得以维持。研究人员将在这一新的生态进化框架的基础上，开发一种预测数学理论，以理解关键的宿主和病原体特征，以及驱动年龄特异性疾病易感性进化的反馈。然后，为了确定这些年龄特异性选择压力是如何在现实世界系统中实例化的，并测试模型的关键预测，研究小组将利用模型植物疾病系统，即白色锦葵（Silene latifolia）上的花药黑穗病（Microbotryum）来量化在一系列疾病频率下年龄特异性抗性的适应性成本、收益和进化潜力。为了增加拟议工作的广泛影响和社会效益，研究人员将与当地自然历史学会合作，对“微真菌”的分布和多样性进行原创性的科学研究，并为本科生提供有意义的研究机会。该奖项反映了美国国家科学基金会的法定使命，并通过使用基金会的知识价值和更广泛的影响审查标准进行评估，被认为值得支持。

When a disease epidemic sweeps through a population of plants, animals, or humans, the youngest individuals in the population are often hardest hit. This is because juveniles are typically more susceptible to infectious disease than adults. Indeed, the spread of many human diseases such as measles and chicken pox is largely driven by children. Likewise in many wildlife species, the spring ‘pulse’ of new highly susceptible young can drive epidemics, including diseases that risk spilling over into human or livestock populations. However, we lack a basic understanding of why juveniles are inherently so susceptible, even after accounting for prior exposure to disease. This research will use mathematical models and experiments with a model plant system to investigate the fundamental ecological and evolutionary processes driving the evolution of age-specific susceptibility. The results will substantially increase our understanding of the feedbacks between resistance evolution and disease spread, which will improve management strategies for wildlife disease, and inform crop breeding for disease resistance. The research will also increase public understanding of science and enrich local biodiversity records and museum collections through new citizen science outreach activities that are integrated with the basic research. The question of why juveniles are so susceptible to disease is puzzling from an evolutionary perspective because infection prior to reproduction would seem to have a much greater negative impact on a host than infection later in life (after the host has had a chance to reproduce). Natural selection should therefore favor individuals that are less susceptible to disease when they are young. This project will test the novel hypothesis that juvenile susceptibility is maintained by feedbacks between evolutionary change in host resistance and ecological change in disease abundance. These “eco-evolutionary” feedbacks occur because the evolution of disease resistance at any age in the host population, can in turn reduce the intensity of disease epidemics. Critically, lower disease-levels make it less likely that a host will encounter disease as a juvenile, thereby allowing the maintenance of juvenile susceptibility. The researchers will build on this novel eco-evolutionary framework to develop a predictive mathematical theory for understanding key host and pathogen traits, and the feedbacks driving the evolution of age-specific disease susceptibility. Then to establish how these age-specific selection pressures are instantiated in a real-world system and to test key predictions from the model, the research team will utilize the model plant-disease system, anther-smut (Microbotryum) on white campion (Silene latifolia) to quantify the fitness costs, benefits, and evolutionary potential of age-specific resistance under a range of disease frequencies. To increase the broader impacts and societal benefits of the proposed work the researchers will engage local natural history societies in original scientific research on the distribution and diversity of ‘micro-fungi’, and provide meaningful research opportunities for undergraduates.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.