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

所有动物和植物都受到天敌——病原体、寄生虫和捕食者——的攻击，由此造成的死亡率和发病率推动了生态和进化的变化。事实上，许多动物的生物学都是由自然选择驱动的，以避免或减轻天敌攻击的影响，以身体表面的防御来击退入侵者，内部的防御来清除攻击者或减少造成的伤害。最常见的是，我们认为防御系统编码在动物的基因组中。自然选择将导致提供抵抗的基因变异在攻击常见时频率增加，在没有攻击的情况下代价高昂时频率下降。然而，最近的研究发现，生活在动物体内的共生细菌也可以保护动物免受攻击。在昆虫中，这些保护性共生体通常是由母亲传给后代的，所以它们的行为就像遗传特征一样。攻击者的存在意味着携带共生体的个体会留下更多的后代，因此自然选择增加了共生体的频率。动物种群可以通过基因组的变化和共生体的扩散来进化出抵抗攻击的能力，这一发现提出了根本性的进化问题。然而，由于这两个过程是单独研究的，我们对它们如何相互作用和区别知之甚少。为了解决我们知识上的这一空白，我们建议研究基因和保护性共生体如何促进实验室果蝇种群对寄生蜂的抗性进化。我们的第一个目标是了解不同的保护模式如何在个人和群体中相互作用。如果这两种变异都存在，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哪种抗性模式的发展。然后，我们将研究共生体防御的两个方面，使它们与基因组中的防御不同，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其宿主有多重作用——除了保护作用，它们可以提供营养，改变热耐受性，并有利于产生女儿而不是儿子。正是这些特征的结合推动了共生体在种群内的传播，因此多重效应可能有利于保护性共生体防御基因组中的基因。我们将通过研究性别比例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验证这一假设。第二个区别是，共生体介导的保护性防御是一种不寻常的特征。它不是简单的“关”或“开”，而是效率取决于存在的细菌数量，就像一支军队的士兵越多，效率就越高。共生体的数量会受到环境的影响，重要的是，它们可以在世代之间传播。一个有很多细菌并且防御良好的雌性会生出同样有很多细菌并且防御良好的女儿。这种不寻常的排列意味着自然选择可能对细菌的数量起作用。因此，我们的最终目的是研究共生滴度及其对寄生虫攻击的进化反应的影响程度。自然选择作用于滴度吗？这些影响会持续几代人吗？这个过程是否产生了对寄生虫威胁水平的耐药性的密切跟踪？这项研究将首次调查这两种防御模式的存在如何影响抗性进化。所获得的了解将有助于预测害虫和病媒对攻击的进化反应，这将使我们了解蚊子和其他病媒的生物防治和疾病传播。

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.