Symbionts or genes? Integrating the evolutionary response to parasites across varying modalities of resistance.

所有动植物都受到天敌--病原体、寄生虫和捕食者--的攻击，由此导致的死亡率和发病率推动了生态和进化的变化。事实上，许多动物生物学是由自然选择驱动的，以避免或减轻天敌攻击的影响，其形式是在身体表面防御以击退入侵者，并在体内防御以清除攻击者或减少造成的损害。最常见的是，我们认为防御系统编码在动物的基因组中。自然选择将导致遗传变异，当攻击常见时，这些变异提供抵抗增加的频率，如果在没有攻击的情况下，它们的代价很高，则会下降。然而，最近的研究发现，生活在动物体内的共生细菌也可以提供抵御攻击的保护。在昆虫中，这些保护性共生体通常是从母亲传给后代的，因此它们的行为像是遗传特征。攻击者的存在将意味着携带共生体的个体会留下更多的后代，因此自然选择会增加共生体的出现频率。动物种群可以进化出对基因组变化和共生体传播的攻击的抵抗力，这一发现引发了根本的进化问题。然而，由于这两个过程是孤立地研究的，我们对它们是如何相互作用和不同的了解很少。为了解决我们知识中的这一差距，我们建议研究基因和保护性共生体如何在果蝇实验室种群中对寄生蜂的抗性进化做出贡献。我们的第一个目标是了解不同的保护模式如何在个人和人群中相互作用。如果两种类型的变异都存在，是否会进化出更强的抵抗力？环境因素，如温度和食物压力，对不同的抗性模式有非常不同的影响。因此，我们将测试环境是否决定了抗性的进化模式。然后，我们将研究共生体防御的两个方面，这两个方面使它们有别于基因组中的防御，并确定这些方面如何影响防御的进化。第一个区别是，保护性共生体通常对寄主以外的保护有多种影响，它们可以提供营养益处，改变热耐性，并且比起男孩更有利于生育女儿。正是这些特征的结合推动了共生体在种群中传播，因此多重效应可能有利于共生体的保护性防御，而不是基因组中的基因。我们将通过研究性别比扭曲如何在抗性进化过程中改变基因和共生体之间的平衡来检验这一假设。第二个区别是保护性共生体介导的防御是一种不寻常的特征。它不是简单的“关闭”或“打开”，而是效率取决于存在的细菌数量，就像一支军队包含更多士兵时更有效一样。共生菌的数量(滴度)可能会受到环境的影响，更重要的是，可以在世代之间传播。雌性如果有很多细菌并且有很好的防御能力，她会生出同样有很多细菌并且有很好防御能力的女儿。这种不同寻常的安排意味着自然选择可能会影响细菌的数量。因此，我们的最终目标是研究共生菌滴度及其对寄生虫攻击的进化反应的影响程度。自然选择会影响滴度吗？这些影响会代代相传吗？这个过程是否产生了对寄生虫威胁水平的抵抗力的密切跟踪？这项研究将是关于这两种防御模式的存在如何塑造抗性进化的首次调查。所获得的了解将有助于预测害虫和媒介对攻击的进化反应，这将为我们了解蚊子和其他媒介的生物防治和疾病传播提供信息。

All animals and plants are attacked by natural enemies - pathogens, parasites and predators - and the resulting mortality and morbidity drives ecological and evolutionary change. Indeed, much of animal biology is driven by natural selection to avoid or mitigate the impact of natural enemy attack, in the form of defences at the body surface to repel invaders, and defences within to clear attackers or reduce the damage caused. Most commonly, we think of defence systems as encoded in an animal's genome. Natural selection will cause genetic variants that provide resistance to increase in frequency when attack is common, and decline if they are costly in the absence of attack. However, recent work has found that symbiotic bacteria living within the animal can also provide protection against attack. In insects, these protective symbionts are commonly passed from mother to offspring, so they behave like genetic traits. The presence of attackers will mean individuals carrying the symbiont leave more offspring, and thus natural selection increases the frequency of the symbiont. The discovery that animal populations can evolve resistance to attack by both changes to the genome and by the spread of symbionts raises fundamental evolutionary questions. However, because the two processes have been studied in isolation, we have little understanding of how they interact and differ. To address this gap in our knowledge, we propose to study how genes and protective symbionts contribute to the evolution of resistance to parasitic wasps in laboratory populations of fruit flies. Our first aim is to understand how different modes of protection interact within individuals and populations. If both types of variation exist, does stronger resistance evolve? Environmental factors, like temperature and food stress, have very different effects on the different modes of resistance. We will therefore test whether the environment determines which mode of resistance evolves.We will then examine two aspects of symbiont defence that make them distinct from defence within the genome, and determine how these impact the evolution of defence. The first distinction is that protective symbionts typically have multiple effects on their host - aside protection, they can provide nutritional benefits, alter thermal tolerance, and favour the production of daughters over sons. It is the combination of these traits that drive symbionts to spread within populations, and multiple effects thus potentially favour protective symbionts defences over genes in the genome. We will test this hypothesis by examining how sex ratio distortion shifts the balance between genes and symbionts during the evolution of resistance.The second distinction is that protective symbiont mediated defence is an unusual trait. It is not simply 'off' or 'on', but the efficiency depends on the number of bacteria present, like an army is more effective when it contains more soldiers. The number of symbionts ('titre') can be affected by the environment, and importantly, can be transmitted between generations. A female who has many bacteria and is well defended produces daughters who likewise have many bacteria and are well defended. This unusual arrangement means that natural selection may act on the number of bacteria. Our final aim therefore is to investigate symbiont titre and the degree to which it impacts on the evolutionary response to parasite attack. Does natural selection act on titre? Do these effects last over generations? Does this process produce close tracking of resistance to the parasite threat level? This study will be the first investigation of how the existence of these two defence modes shapes resistance evolution. The understanding gained will aid prediction of the evolutionary responses of pests and vectors to attack, which will inform our understanding of biocontrol and disease transmission by mosquitoes and other vectors.