The evolution of parasitic sex ratio distortion

宿主-寄生虫的相互作用在整个自然界中无处不在，形成了动植物群落的重要组成部分。其中，扭曲宿主性别比例的寄生虫在无脊椎动物中广泛存在。性别比扭曲者的影响可能会对生物多样性产生强大的影响；它们可能导致种群灭绝，并改变群落中动物的组成。此外，由于它们既可以影响有益的宿主，也可以影响有害的宿主，目前人们对利用这种寄生虫进行生物防治非常感兴趣。性别比扭曲在不同的寄生虫(真核生物和细菌)中进化，并影响不同的宿主。为什么要扭曲性别比例呢？这些寄生虫在卵中从母亲传给后代，只由雌性传播。这些寄生虫进化出了一些策略，以增加女性宿主的相对频率(从而增加了寄生虫的传播)。女性化是由细菌沃尔巴克氏菌和甲壳动物中的微孢子虫(真核寄生虫)诱导的。相比之下，沃尔巴克氏杆菌会导致昆虫的雄性死亡。发现雄性杀死和雌性化的机制是理解宿主和寄生虫共同进化的关键。我们认为，这些细胞内寄生虫最有可能的作用方式是将分子分泌到宿主细胞中，然后影响宿主的分子通路，它们可能改变对外部激素信号的反应，甚至诱导细胞程序性死亡(凋亡)。这种变化可能会扰乱性发育模式，或导致特定性别的胚胎死亡。目的：我们将通过测试以下假设来研究远缘寄生虫性别比扭曲的进化：相似的机制导致沃尔巴克氏菌(昆虫宿主中的雄性杀死，甲壳类宿主中的雌性化)不同的性操纵策略-在远亲寄生虫(沃尔巴克氏菌和微孢子虫)中进化出平行的雌性化机制。目标1.我们将研究沃尔巴克氏菌诱导的雄性杀死和雌性化的分子基础。我们将使用最先进的技术(蛋白质组学)来识别分泌到宿主细胞质中的导致女性化或男性死亡的分子，并跟踪它们在宿主中诱导的变化。我们将首先在果蝇(果蝇)/沃尔巴克氏菌雄性杀死系统中研究这一点。这两种生物的基因组都是已知的，将帮助我们识别蛋白质及其功能。然后，我们将继续研究在甲壳类动物青春藤(林虱)中雌性化的沃尔巴克氏菌。我们将通过测试发育中的寄主寄生虫中的细胞死亡模式的操纵来研究沃尔巴克氏杆菌和微孢子虫诱导雌性化的细胞基础。为了确定作用地点，我们将绘制微孢子虫雌性化和沃尔巴克氏菌在甲壳类宿主性别分化期间的分布。我们最近观察到了沃尔巴克氏菌对果蝇雄性的杀灭与细胞凋亡(程序性细胞死亡)之间的关系。我们将测试雌性化的寄生虫是否也会诱导生殖腺中的细胞凋亡，以使宿主雌性化。

Host-parasite interactions are pervasive throughout the natural world, forming a critical component of plant and animal communities. Among them, parasites that distort host sex ratios are widespread in invertebrates. The effect of sex ratio distorters can have a powerful effect on biodiversity; they can cause populations to become extinct and change the composition of animals in the community. Additionally as they can affect harmful as well as beneficial hosts, there is currently a great deal of interest in the use of such parasites for biological control. Sex ratio distortion has evolved in diverse parasites (eukaryotes and bacteria) and affects diverse hosts. Why distort sex ratio? These parasites are passed from mother to offspring in the eggs and are only transmitted by females. These parasites have evolved a number of strategies to increase the relative frequency of female hosts (so increasing the spread of the parasite). Feminisation is induced by the bacterium Wolbachia and by microsporidia (eukaryotic parasites) in Crustacea. In contrast Wolbachia causes male killing in insects. Discovering the mechanisms of male killing and feminisation is key to understanding host-parasite coevolution. We propose that these intracellular parasites are most likely to act by secreting molecules into the host cell which will then influence host molecular pathways, they may modify the response to external hormonal signals or even induce programmed cell death (apoptosis). Such changes could disrupt patterns of sexual development or lead to sex-specific embryo mortality. AIMS: We will investigate the evolution of sex ratio distortion in distantly related parasites by testing the hypotheses that - Similar mechanisms lead to contrasting strategies of sexual manipulation by Wolbachia (male killing in insect hosts, feminisation in crustacean hosts) - Parallel mechanisms of feminisation have evolved in distantly related parasites (Wolbachia and microsporidia) OBJECTIVES I. WE WILL INVESTIGATE THE MOLECULAR BASIS OF WOLBACHIA INDUCED MALE KILLING AND FEMINISATION. We will use state of the art techniques (proteomics) to identify molecules secreted into the host cytoplasm that cause feminisation or male killing, and to follow the changes they induce in the host. We will study this initially in the Drosophila (fruit fly)/Wolbachia male killing system. The genome of both these organisms is known and will help us to identify proteins and their function. We will then go on to study feminising Wolbachia in the crustacean Armadillidium vulgare (woodlouse). II. WE WILL INVESTIGATE THE CELLULAR BASIS OF WOLBACHIA AND MICROSPORIDIA INDUCED FEMINISATION BY TESTING FOR MANIPULATION OF THE PATTERN OF CELL DEATH IN THE DEVELOPING HOST Parasites cause feminisation in Crustacea by inhibiting development of the androgenic gland (the gland that controls male sexual differentiation). To pinpoint the site of action, we will map the distribution of feminising microsporidia and Wolbachia during sexual differentiation of their crustacean hosts. We have recently observed an association between male killing in Drosophila bifasciata by Wolbachia and apoptosis (programmed cell death). We will test whether feminising parasites also induce apoptosis in the androgenic gland in order to feminise the host.