Strength in diversity: the effects of host-parasite genetic diversity on transmission and evolution

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Parasites are a dominant force in nature. Perhaps as many as half of all species have a parasitic lifestyle and they have powerful effects on the fitness of the organisms they infect. Many studies of host-parasite interactions have considered only the simplest scenario of a single parasite infecting a single host genotype. However, most host-parasite interactions are far more complex than this. Host populations are made up of a diversity of genotypes that will vary in their resistance to parasites. Parasite infections commonly consist of multiple strains of parasite that will vary in virulence. The interaction is not always straightforward, with, for example, parasites that are virulent in one host genotype, relative to other parasites strains, being relatively less virulent in another host genotype. When infections involve multiple parasite strains, they compete to exploit the limited resources provided by the host, with the most virulent strains being likely to win. Most models therefore predict that within-host competition between parasite strains results in an infection expressing greater virulence, and will also select over evolutionary time for parasites of greater virulence. However, experimental evidence for these effects is limited and contradictory, with some studies finding that less virulent strains in fact win during within-host competition or that the outcome is dependent on the host genotype in which the competition takes place. This project will investigate the effects of both host and parasite genetic diversity on parasite virulence, transmission and evolution, in honeybees and their fungal parasite, chalkbrood. Honeybees are an excellent model host because, unusually for a social insect, their colonies have relatively high genetic diversity. This makes the identification of genetic effects on resistance straightforward to identify and has been suggested to have evolved to improve their resistance to disease. The chalkbrood parasite is also an excellent model because it produces a single batch of characteristic spores shortly after killing its host, which makes parasite fitness easy to measure. Chalkbrood also has an intriguing reproductive biology, requiring mating between two opposite 'sex' strains to reproduce. Whereas within-host interactions between most parasites are competitive, for chalkbrood they may therefore be either competitive or mutualistic depending upon the sexes of the interacting strains. The project will combine advanced apicultural, microbiological and genetic techniques to examine how honeybee and chalkbrood genetic diversity determines the outcome of infections. It will use a powerful genetic method to quantify the actual within-host dynamics of infections involving multiple parasite strains. Finally it will carry out experimental evolution to establish how host and parasite genetic diversity impacts the evolution of the chalkbrood parasite. Recent epidemics, such as of the Varroa parasite and Colony Collapse Disorder, have highlighted the vulnerability of honeybees to disease, but honeybees suffer from a number of widespread endemic parasites, such as chalkbrood, that also significantly reduce their fitness and productivity. Honeybees are estimated to pollinate crops worth £200 million per annum in the UK, as well as many endangered plant species, so managing their populations sustainably is important for both natural ecosystems and agriculture in the UK. The threat of disease is the principle concern of UK beekeepers today. The results of the project will therefore help inform management strategies, as well as significantly advancing our understanding of the evolutionary biology of host-parasite interactions in general.