Strength in diversity: the effects of host-parasite genetic diversity on transmission and evolution

寄生虫是自然界的主导力量。也许多达一半的物种都有寄生的生活方式，它们对被它们感染的生物体的适应性有很大的影响。许多关于宿主-寄生虫相互作用的研究只考虑了单一寄生虫感染单一宿主基因型的最简单情况。然而，大多数宿主-寄生虫相互作用远比这复杂得多。宿主种群由多种基因型组成，这些基因型对寄生虫的抵抗力各不相同。寄生虫感染通常由多株毒性不同的寄生虫组成。这种相互作用并不总是直接的，例如，相对于其他寄生虫菌株，在一种宿主基因型中具有毒性的寄生虫，在另一种宿主基因型中毒性相对较弱。当感染涉及多种寄生虫菌株时，它们会竞争利用宿主提供的有限资源，毒性最强的菌株可能会获胜。因此，大多数模型预测宿主内寄生虫菌株之间的竞争会导致表现出更大毒力的感染，并且在进化过程中也会选择更大毒力的寄生虫。然而，这些影响的实验证据是有限和矛盾的，一些研究发现，在宿主内部竞争中，毒性较低的菌株实际上获胜，或者结果取决于发生竞争的宿主基因型。本项目将研究寄主和寄生物遗传多样性对蜜蜂及其真菌寄生物白垩菌的毒力、传播和进化的影响。蜜蜂是一个很好的寄主模式，因为它们的群体具有相对较高的遗传多样性，这对群居昆虫来说是不寻常的。这使得确定对抗性的遗传影响变得简单明了，并已被认为是为了提高它们对疾病的抵抗力而进化的。白垩寄生体也是一个很好的模型，因为它在杀死宿主后不久就会产生一批有特征的孢子，这使得寄生虫的适应性很容易测量。白垩白菌还有一种有趣的生殖生物学特性，需要两种异性交配才能繁殖。在宿主内，大多数寄生虫之间的相互作用是竞争性的，而对于白垩菌来说，根据相互作用菌株的性别，它们可能是竞争性的，也可能是互惠性的。该项目将结合先进的养蜂业、微生物学和遗传技术，研究蜜蜂和白垩菌的遗传多样性如何决定感染的结果。它将使用一种强大的遗传方法来量化涉及多种寄生虫菌株的宿主内感染的实际动态。最后将进行实验进化，以确定寄主和寄生虫遗传多样性如何影响白垩巢寄生虫的进化。最近的流行病，如瓦罗阿寄生虫和蜂群衰竭失调症，突出了蜜蜂对疾病的脆弱性，但蜜蜂也受到许多广泛存在的地方性寄生虫的影响，如白垩病，这也大大降低了它们的适应性和生产力。据估计，在英国，蜜蜂每年为价值2亿英镑的农作物以及许多濒危植物授粉，因此可持续地管理它们的数量对英国的自然生态系统和农业都很重要。疾病的威胁是当今英国养蜂人最关心的问题。因此，该项目的结果将有助于为管理策略提供信息，并大大提高我们对宿主-寄生虫相互作用的进化生物学的理解。

Parasites are a dominant force in nature. Perhaps as many as half of all species have a parasitic lifestyle and they have powerful effects on the fitness of the organisms they infect. Many studies of host-parasite interactions have considered only the simplest scenario of a single parasite infecting a single host genotype. However, most host-parasite interactions are far more complex than this. Host populations are made up of a diversity of genotypes that will vary in their resistance to parasites. Parasite infections commonly consist of multiple strains of parasite that will vary in virulence. The interaction is not always straightforward, with, for example, parasites that are virulent in one host genotype, relative to other parasites strains, being relatively less virulent in another host genotype. When infections involve multiple parasite strains, they compete to exploit the limited resources provided by the host, with the most virulent strains being likely to win. Most models therefore predict that within-host competition between parasite strains results in an infection expressing greater virulence, and will also select over evolutionary time for parasites of greater virulence. However, experimental evidence for these effects is limited and contradictory, with some studies finding that less virulent strains in fact win during within-host competition or that the outcome is dependent on the host genotype in which the competition takes place. This project will investigate the effects of both host and parasite genetic diversity on parasite virulence, transmission and evolution, in honeybees and their fungal parasite, chalkbrood. Honeybees are an excellent model host because, unusually for a social insect, their colonies have relatively high genetic diversity. This makes the identification of genetic effects on resistance straightforward to identify and has been suggested to have evolved to improve their resistance to disease. The chalkbrood parasite is also an excellent model because it produces a single batch of characteristic spores shortly after killing its host, which makes parasite fitness easy to measure. Chalkbrood also has an intriguing reproductive biology, requiring mating between two opposite 'sex' strains to reproduce. Whereas within-host interactions between most parasites are competitive, for chalkbrood they may therefore be either competitive or mutualistic depending upon the sexes of the interacting strains. The project will combine advanced apicultural, microbiological and genetic techniques to examine how honeybee and chalkbrood genetic diversity determines the outcome of infections. It will use a powerful genetic method to quantify the actual within-host dynamics of infections involving multiple parasite strains. Finally it will carry out experimental evolution to establish how host and parasite genetic diversity impacts the evolution of the chalkbrood parasite. Recent epidemics, such as of the Varroa parasite and Colony Collapse Disorder, have highlighted the vulnerability of honeybees to disease, but honeybees suffer from a number of widespread endemic parasites, such as chalkbrood, that also significantly reduce their fitness and productivity. Honeybees are estimated to pollinate crops worth £200 million per annum in the UK, as well as many endangered plant species, so managing their populations sustainably is important for both natural ecosystems and agriculture in the UK. The threat of disease is the principle concern of UK beekeepers today. The results of the project will therefore help inform management strategies, as well as significantly advancing our understanding of the evolutionary biology of host-parasite interactions in general.