CAREER: The contributions of imperfect transmission and cytoplasmic incompatibility to Wolbachia frequency variation

10亿多年前，宿主细胞吞噬了一种自由生活的细菌，这一非凡的事件导致了线粒体的进化，线粒体现在为动物、植物和真菌细胞提供化学能量。最近的研究表明，微生物在其他物种的细胞内栖息的过程(称为内共生)非常常见，特别是在昆虫中。例如，一种名为沃尔巴克氏菌的微生物感染了地球上一半以上的昆虫物种。与线粒体不同，沃尔巴克氏菌通常不是宿主生存和繁殖所必需的。相反，由于未知的原因，宿主物种中携带沃尔巴克氏菌的个体比例在任何时候都有很大差异，这使得很难预测对宿主生物学的影响。这个项目将揭开沃尔巴克氏菌流行变异的原因，为更广泛地理解有利于内共生的条件提供一个模型。这项工作还可能有助于改善人类健康。沃尔巴克氏菌可以在蚊子系统中阻止登革热和寨卡病毒等病毒，但要提高这项工作的效率，需要确定有利于沃尔巴克氏菌高流行的条件。这个项目将在自然系统中确定这样的条件。在当地，该项目将在尖端实验室、现场和计算方法方面教育和培训第一代和蒙大拿州原住民学生，以提高他们在STEM相关职业中的竞争力。蒙大拿大学将进一步开发一门侧重于宿主-微生物相互作用的新课程，以包括旨在使蒙大拿州农村地区的个人接触独特的内共生生物学的外联活动。生物体的表现和适合性取决于生物组织各层次之间的相互作用。在所有物种的相互作用中，动物与生活在其细胞内的微生物内共生体之间的相互作用可能是最密切的，影响宿主的行为、生理、生活史和适合性。一些内共生菌甚至可能有助于生殖隔离和物种形成，突出了它们对寄主生物学的广泛重要性。宿主-内共生菌相互作用的进化结果最终取决于宿主种群中内共生菌的流行率，由于未知原因，宿主种群内共生菌的流行率差异很大。该项目将利用分布在不同寄主物种上的5000万年沃尔巴克氏菌进化来确定沃尔巴克氏菌频率变异的原因。该项目将具体分析宿主和内共生菌基因组中的基因如何相互作用以及如何与温度相互作用(GxGxE相互作用)，以影响母体沃尔巴克氏菌的传播率和沃尔巴克氏菌诱导的生殖操纵(如细胞质不亲和性)的强度。然后将使用数学模型来评估基因组和环境相互作用如何导致沃尔巴克氏菌在不同宿主系统中的流行。在每一步，该项目都将包括利用独特的内共生生物学来教育和培训蒙大拿州的第一代和原住民学生的活动。该奖项反映了NSF的法定使命，并通过使用基金会的智力优势和更广泛的影响审查标准进行评估，被认为值得支持。

Over a billion years ago a host cell engulfed a free-living bacterium in a remarkable event that led to the evolution of mitochondria that now provide the chemical energy for animal, plant, and fungal cells. Recent research has revealed that the process of microbes taking up residence inside the cells of other species (known as endosymbiosis) is very common, especially among insects. For example, a single microbe called Wolbachia infects more than half of all insect species on Earth. Unlike mitochondria, Wolbachia are usually not required for their hosts to survive and reproduce. Instead, the proportion of individuals within a host species with Wolbachia at any time varies greatly for unknown reasons, making it hard to predict the consequences for host biology. This project will unravel the causes of variable Wolbachia prevalence as a model for more broadly understanding conditions that favor endosymbiosis. This work will also potentially contribute to improving human health. Wolbachia can block viruses like dengue and Zika in mosquito systems, but increasing the efficacy of this work requires identifying conditions that favor high Wolbachia prevalence. This project will identify such conditions in natural systems. Locally, this project will educate and train first-generation and Native Montana students in cutting-edge laboratory, field, and computational approaches that will improve their competitiveness in STEM-related careers. A new course at the University of Montana focused on host-microbe interactions will be further developed to include outreach activities aimed at exposing individuals in rural Montana to the unique biology of endosymbiosis. Organismal performance and fitness depends on interactions across levels of biological organization. Among all species interactions, those between animals and microbial endosymbionts that live inside their cells are perhaps the most intimate, influencing host behavior, physiology, life history, and fitness. Some endosymbionts may even contribute to reproductive isolation and speciation, highlighting their broad importance for host biology. The evolutionary outcomes of host-endosymbiont interactions ultimately depend on endosymbiont prevalence in host populations, which varies widely for unknown reasons. This project will leverage 50 million years of Wolbachia evolution distributed across divergent host species to determine the causes of Wolbachia frequency variation. The project will specifically dissect how genes in host and endosymbiont genomes interact with each other and with temperature (GxGxE interactions) to influence maternal Wolbachia transmission rates and the strength of Wolbachia-induced reproductive manipulations like cytoplasmic incompatibility. Mathematical models will then be used to evaluate how both genomic and environmental interactions contribute to Wolbachia prevalence in divergent host systems. At each step, this project includes activities that will leverage the unique biology of endosymbiosis to educate and train first-generation and Native students in Montana.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.