The evolution of parasitic sex ratio distortion

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.