Male-killing symbiosis across a predator-prey interaction: a genomic and experimental approach

捕食者与猎物相互作用中的雄性致死共生：基因组和实验方法

• 批准号: NE/X010171/1
• 负责人: Ailsa McLean
• 金额: $ 9.73万
• 依托单位: University of Oxford
• 依托单位国家: 英国
• 项目类别: Research Grant
• 财政年份: 2023
• 资助国家: 英国
• 起止时间: 2023 至 无数据
• 项目状态: 未结题
• 来源: https://gtr.ukri.org/projects?ref=NE%2FX010171%2F1
• 关键词: Male; killing; symbiosis; across; predator

Most insects carry specialised bacteria that dwell permanently inside them. These bacteria are known as symbionts and may be beneficial or costly to their insect host. In this project, we will investigate a bacterial symbiont, Spiroplasma, that is able to manipulate host insect reproduction to its own advantage.Like many insect symbionts, Spiroplasma is predominantly transmitted from female insects to their offspring. Because males cannot transmit the bacteria, they are essentially an evolutionary 'dead end' from the perspective of the symbiont. Symbionts are therefore under selection to increase the proportion of female offspring, and the result is a diversity of symbiont-induced reproductive manipulation strategies. Spiroplasma employs one of the most straightforward: male offspring carrying the symbiont die before adulthood (usually in the egg stage). This is assumed to benefit the surviving sisters, although the advantages are not always clear.In addition to maternal transmission, symbionts can occasionally be transmitted between unrelated individuals, either within or between species. This 'horizontal' transmission is evolutionarily important because it is a route for heritable characteristics to be passed across species boundaries in animals. However, since such transfers are rare in nature, we know little about the process. In this project, we will study two closely-related groups of Spiroplasma, infecting ladybirds and aphids respectively, in order to ask what happens when symbionts move between distantly-related insects.First, we will sequence the genomes of 13 strains of Spiroplasma bacteria: three from different species of ladybirds, and 10 from the pea aphid. The pea aphid strains will include bacteria causing complete, partial and no death of male offspring. We will use the genomes to look for similarities and differences among the Spiroplasma strains in the putative genetic mechanism for male-killing. We also aim to identify the genetic variation that drives the phenotypic differences in male-killing seen among the aphid Spiroplasma. In the second part of the project, we will recreate a likely route of symbiont transmission. Ladybirds are well-known as predators of aphids, and it is highly plausible that this predator-prey relationship allowed transmission of Spiroplasma between the two groups in their evolutionary past. We will carry out microinjection of body fluid containing male-killing Spiroplasma from aphids to ladybirds, and vice versa. We will test whether a new heritable infection is established and if the new infections cause male-killing. Our study combines an ambitious plan to recreate cross-species symbiont transmission with a detailed understanding of mechanism through symbiont genome sequencing. Ladybirds and aphids present a great opportunity to understand horizontal acquisition of traits via horizontal transmission of symbionts, and also to investigate the barriers that may stand in the way of that transfer. By gaining a full picture of symbiont function and transmission in the context of one specific predator-prey interaction, we will open the way to answer further questions surrounding the acquisition of novel symbionts, and the evolution of symbiont-mediated effects. Insects are an extraordinary evolutionary success story. Hidden inside insects, bacterial symbionts play important roles in nutrition, defence and reproduction. Explaining how and why new symbiotic associations arise is therefore a vital element for understanding insect evolution, and is the overarching aim of the project we propose.

大多数昆虫都携带着专门的细菌，这些细菌会永久居住在它们体内。这些细菌被称为共生体，可能对它们的昆虫宿主有益，也可能代价高昂。在这个项目中，我们将研究一种细菌共生体，螺原体，它能够操纵宿主昆虫的繁殖以达到自己的优势。像许多昆虫共生体一样，螺原体主要由雌性昆虫传播给它们的后代。因为雄性不能传播细菌，从共生体的角度来看，它们本质上是进化的“死胡同”。因此，共生体在选择中增加了雌性后代的比例，结果是共生体诱导的生殖操纵策略的多样性。螺原体采用了一种最直接的方法：携带共生体的雄性后代在成年前死亡（通常在卵期）。这被认为有利于幸存的姐妹，尽管优势并不总是明确的。除了母体传播外，共生体偶尔也会在不相关的个体之间传播，无论是在物种内部还是物种之间。这种“水平”传播在进化上是重要的，因为它是动物遗传特征跨物种传播的途径。然而，由于这种转移在自然界中很罕见，我们对这一过程知之甚少。在这个项目中，我们将研究两个密切相关的螺原体，分别感染瓢虫和蚜虫，以了解当共生体在远亲昆虫之间移动时会发生什么。首先，我们将对13株螺原体细菌进行基因组测序：3株来自不同种类的瓢虫，10株来自豌豆蚜虫。豌豆蚜虫菌株包括导致雄性后代完全死亡、部分死亡和不死亡的细菌。我们将使用基因组来寻找螺旋体菌株在假定的雄性死亡遗传机制中的异同点。我们还旨在确定驱动在蚜虫螺旋体中看到的雄性杀死表型差异的遗传变异。在项目的第二部分，我们将重建一个可能的共生体传播途径。众所周知，瓢虫是蚜虫的捕食者，这种捕食者-被捕食者的关系使得螺原体在两个种群之间的进化过程中得以传播，这是非常可信的。我们将从蚜虫向瓢虫注射含有杀雄螺原体的体液，反之亦然。我们将测试是否建立了新的遗传感染，以及新的感染是否导致男性死亡。我们的研究结合了一个雄心勃勃的计划，即重建跨物种的共生传播，并通过共生基因组测序详细了解机制。瓢虫和蚜虫提供了一个很好的机会来了解通过共生体的水平传播而获得的特征，同时也研究了可能阻碍这种转移的障碍。通过在一个特定的捕食者-猎物相互作用的背景下获得共生体功能和传播的全貌，我们将为回答围绕新共生体的获得和共生体介导效应的进化的进一步问题开辟道路。昆虫是一个非凡的进化成功故事。隐藏在昆虫体内的细菌共生体在营养、防御和繁殖方面发挥着重要作用。因此，解释新的共生关联如何以及为什么产生是理解昆虫进化的重要因素，也是我们提出的项目的总体目标。