OSIB: DYNAMIC INTERACTIONS BETWEEN HOST SOCIAL BEHAVIOR AND PARASITE VIRULENCE

传染病对人类和我们赖以生存的动植物构成根本威胁。正如2019冠状病毒病大流行所表明的那样，传染病疫情的发展主要取决于宿主的行为：宿主之间的社会互动越多，导致此类疾病的寄生虫传播速度就越快。我们通常认为，这种更快的传播导致大量混合良好的寄生虫种群，具有快速进化增加“毒力”的潜力，即它们杀死宿主的速度。然而，支持这些假设的有力证据很少，而且有几个复杂的因素。首先，动物在应对疫情时往往“保持社会距离”，减少传播，并可能影响寄生虫种群及其进化。其次，保持社交距离的程度可能取决于寄生虫的毒力。第三，在鸟类、哺乳动物和鱼类中，更多的社会性宿主个体往往能够更好地限制寄生虫的生长，并且可能不太可能传播它们的感染。为了揭示宿主社会行为、寄生虫传播和毒力进化之间复杂的相互作用，研究小组将整合数学模型、实验流行病和自然流行病调查。他们将使用特立尼达孔雀鱼和一种生长在其皮肤上的寄生虫，对进化流行病学中的许多基本假设进行首次测试。在他们的研究期间，该团队将培训特立尼达的野生动物管理人员和学生，为宾夕法尼亚州的学校开发课程，并培训一组不同的美国科学家。该项目将极大地提高我们预测行为如何影响人类和动物种群的疾病传播和进化的总体能力。宿主行为是我们对传染病动力学理解的最大差距。该项目将为行为、疾病和进化生态学之间的基本相互作用提供独特的见解，这些相互作用共同决定了流行病和寄生虫毒力进化的轨迹。重要的是，研究小组将对宿主社会行为如何驱动寄生虫毒力进化进行首次实验测试。他们将这种大规模实验方法与理论相结合，以评估宿主社会行为、寄生虫传播和毒力进化相互作用的多种动态生态进化途径的相对重要性：每种途径都得到了理论支持，但在任何系统中都缺乏强有力的经验检验。最后，他们将用自然群落的观测数据验证他们的实验和理论建立的总体框架。他们将使用这种综合方法来测试寄主的社会行为如何：1)塑造寄生虫种群的规模和结构；2)通过选择性和非选择性机制驱动寄生虫毒力进化；3)应对疫情以减缓其传播。该团队使用的特立尼达孔雀鱼-旋齿鱼系统使他们能够研究无处不在的生态环境（捕食）如何影响毒力进化：毒力进化研究大多忽略了生态学，但是野生动物病原体从这种环境中传播开来是人类出现疾病的关键途径。所产生的框架将适用于宿主具有社会性、病原体具有传染性、可能发生共感染以及传播和毒性相互权衡的所有系统。这些条件都已在人类病原体中得到证实，并且很可能在各个系统中得到满足。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。

Infectious diseases pose a fundamental threat to humans and the plants and animals we depend on. As demonstrated by the COVID-19 pandemic, how an infectious disease outbreak progresses depends critically on host behavior: the more social interaction between hosts, the faster the parasites that cause such diseases spread. We often assume that this faster spread leads to large, well-mixed parasite populations with high potential for rapid evolutionary increase in ‘virulence’, the rate at which they kill hosts. However, robust evidence supporting these assumptions is rare, and there are several complicating factors. First, animals often ‘socially distance’ in response to an outbreak, reducing transmission, and presumably affecting parasite populations and their evolution. Second, the magnitude of social distancing likely depends on parasite virulence. Third, across birds, mammals, and fish, more social host individuals are often better able to limit parasite growth, and may be less likely to transmit their infection. To unravel the complex interactions between host social behavior, parasite transmission, and virulence evolution, the research team will integrate mathematical models, experimental epidemics, and surveys of natural epidemics. They will use the Trinidadian guppy and a parasitic worm that grows on its skin in the first tests of many fundamental assumptions in evolutionary epidemiology. During their research, the team will train Trinidadian wildlife managers and students, develop curricula for Pennsylvanian schools, and train a diverse group of US-based scientists. The project will dramatically improve our general ability to predict how behavior affects disease spread and evolution across human and animal populations. Host behavior is the single biggest gap in our understanding of infectious disease dynamics. This project will provide unique insight into the fundamental interactions between behavioral, disease and evolutionary ecology that together dictate the trajectory of epidemics and parasite virulence evolution. Importantly, the research team will conduct the first experimental test of how host social behavior drives parasite virulence evolution. They combine this large-scale experimental approach with theory to evaluate the relative importance of the multiple dynamic, eco-evolutionary pathways by which host social behavior, parasite transmission, and virulence evolution interact: each pathway has received theoretical support but lacks robust empirical test in any system. Finally, they will validate the general framework built from their experiment and theory with observational data from natural communities. They will use this integrative approach to test how host social behavior: 1) shapes the size and structure of parasite populations; 2) drives parasite virulence evolution through selective and non-selective mechanisms; 3) responds to an outbreak to slow its spread. The Trinidadian guppy-Gyrodactylus system the team uses allows them to examine how a ubiquitous ecological context, predation, may affect virulence evolution: virulence evolution research mostly ignores ecology, but zoonotic spillover of wildlife pathogens from such contexts is a key route of disease emergence in humans. The framework produced will apply to all systems in which hosts are social, pathogens are contagious, coinfections are possible, and transmission and virulence trade off. These conditions have all been demonstrated in human pathogens and are likely met across systems.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.