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

Lead Research Organisation: University of Sussex
Department Name: Sch of Life Sciences


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.
Description Many parasite infections consist of multiple parasite strains with conflicting interests. The resulting within-host competition between a genetic diversity of parasites is predicted to result in, and select for, increased virulence. Hosts are also genetically diverse, with host genotypes differing in resistance. The outcome of the host-parasite interaction is therefore likely to depend upon the specific host and parasite genotypes involved. This project investigated the effects of both host and parasite genetic diversity on parasite virulence, fitness and evolution using the honeybee, a social insect with colonies that are naturally genetically diverse, and chalkbrood, a heterothallic fungal parasite, as the model system. The key findings of the main project were that: 1) honeybees show significant genetic variation in resistance to the parasites, which relates at least partly to relative expression of immune genes; host genotypic diversity affected 2) the success of parasite transmission and 3) parasite evolution; parasite genetic diversity had complex, strain-specific effects on 4) the outcome of within-host competition and 5) parasite evolution. In addition, the linked PhD studentship discovered that: 6) Aspergillus fungi are common parasites in bee colonies, with variable pathogenicity; 7) pollen diversity and nutritional stress affect the susceptibility of bee larvae to fungal parasites; 8) coinfections of two or more Aspergillus species had synergistic or competitive effects depending upon the combination of species; 9) parasite evolution over serial passages was characterised by an unexpected loss of parasite fitness.
Exploitation Route This was blue-skies research, but the findings do demonstrate that beekeepers are likely to be able to maintain fitter and more productivity bee colonies if they take measures to help ensure their colonies are genetically diverse.
Sectors Agriculture, Food and Drink

Description The work has helped inform beekeepers about the importance of colony genetic diversity for the resistance of honeybees to disease, and also about the potential importance of Aspergillus fungal parasites.
First Year Of Impact 2009
Sector Agriculture, Food and Drink,Education
Impact Types Societal,Economic

Description Panama Science and Innovation Fund
Amount £48,850 (GBP)
Organisation Foreign Commonwealth and Development Office (FCDO) 
Sector Public
Country United Kingdom
Start 07/2015 
End 03/2016
Description International collaboration with Dr Jensen 
Organisation University of Copenhagen
Country Denmark 
Sector Academic/University 
PI Contribution Contributed expertise and resources, and led collaborative research
Collaborator Contribution Contributed expertise and fungal strains, and provided training to members of my research team
Impact Foley, K., Fazio, G., Jensen, A.B. & Hughes, W.O.H. 2014. The distribution of Aspergillus spp. opportunistic parasites in hives and their pathogenicity to honeybees. Vet Microbiol 169:203-210. Evison, S. E. F., Fazio, G., Chappell, P., Foley, K., Jensen, A.B. & Hughes, W.O.H. 2013. Host-parasite genotypic interactions: the dynamics of diversity. Ecol & Evol 3:2214-2222. Foley, K., Fazio, G., Jensen, A. B. & Hughes, W.O.H. 2012. Nutritional limitation and resistance to opportunistic Aspergillus parasites in honey bee larvae. J Invert Pathol 111:68-73.
Start Year 2008