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.

大多数昆虫都携带永久居住在体内的特殊细菌。这些细菌被称为共生体，对其昆虫宿主可能有益，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发挥其自身的优势。像许多昆虫共生体一样，螺原体主要从雌性昆虫传播给它们的后代。由于雄性无法传播细菌，因此从共生体的角度来看，它们本质上是进化的“死胡同”。因此，共生体受到选择以增加雌性后代的比例，其结果是共生体诱导的生殖操纵策略的多样性。螺原体采用最直接的方式之一：携带共生体的雄性后代在成年之前（通常在卵阶段）死亡。人们认为这对幸存的姐妹有利，尽管其优点并不总是很明显。 除了母体传播之外，共生体有时也可以在不相关的个​​体之间传播，无论是在物种内部还是在物种之间。这种“水平”传播在进化上很重要，因为它是动物遗传特征跨越物种边界的途径。然而，由于这种转移在自然界中很少见，我们对这个过程知之甚少。在这个项目中，我们将研究两个密切相关的螺原体菌群，分别感染瓢虫和蚜虫，以了解当共生体在远缘昆虫之间移动时会发生什么。首先，我们将对 13 株螺原体细菌的基因组进行测序：其中 3 株来自不同种类的瓢虫，10 株来自豌豆蚜。豌豆蚜菌株将包含导致雄性后代完全死亡、部分死亡和不死亡的细菌。我们将利用基因组来寻找螺原体菌株之间在假定的雄性致死遗传机制中的相似性和差异。我们还旨在确定导致蚜虫螺原体雄性死亡表型差异的遗传变异。在该项目的第二部分中，我们将重新创建一条可能的共生传播途径。众所周知，瓢虫是蚜虫的捕食者，这种捕食者与被捕食者的关系很可能允许螺原体在其进化过程中在两个群体之间传播。我们将对含有雄性致死螺原体的体液进行显微注射，从蚜虫到瓢虫，反之亦然。我们将测试是否存在新的遗传感染以及新的感染是否会导致男性死亡。我们的研究将重建跨物种共生体传播的雄心勃勃的计划与通过共生体基因组测序对机制的详细了解结合起来。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获得性状，并调查可能阻碍这种转移的障碍。通过在特定的捕食者-猎物相互作用的背景下全面了解共生体的功能和传播，我们将为回答有关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何出现是理解昆虫进化的重要因素，也是我们提出的项目的首要目标。