Are all hosts created equal? Transmission dynamics in a natural multi-host parasite community

Many of the most pressing concerns about emerging infectious disease in humans (eg pandemic influenza, West Nile virus, Hantavirus) and wildlife (eg bovine TB in cattle and badgers, squirrel pox transmission from grey to red squirrels) arise from parasites moving from one host species to another. As such there is considerable interest in how the composition of possible hosts in a community affects whether a disease spreads or not. Each host species can differ in their susceptibility to the parasite, their social structure and/or behaviour, so that the composition of the host community plays a key role in determining why some parasites cause an epidemic (i.e HIV), while others don't (i.e. Ebola). To aid our understanding of these complex, real-world communities, several mathematical models have been developed which show that the contribution each host species makes to the parasite's ability to spread is fundamental in determining whether the disease persists, and the outcome of targeted control. To date, however, these theories have not been tested with actual data, meaning they largely remain abstract conceptual frameworks. In particular, it is not known whether the host species' contributions to disease spread can be determined solely from the number of infected individuals within each host species. This is important as most studies of parasites that infect multiple hosts are likely to be purely observational, because it is logistically or ethically unfeasible to conduct the necessary experiments. However, there may be general guidelines, based on fundamental aspects of host-parasite ecology that can be used to infer these host contributions to parasite transmission and persistence. For example, both the transmission biology of the parasite (ie how it moves from one host to another) and the way host species interact in the community (eg their movement patterns, habitat usage, resource competition etc) will determine how each host species contributes to parasite persistence. Clearly, there is a need to determine whether disease patterns that we see in nature, combined with a basic understanding of host-parasite biology, can be used to predict how parasites will respond to control efforts targeting one host species or another. We will use a highly novel combination of large-scale manipulation experiments and mathematical modelling to measure host species contributions to parasite transmission across a diverse, natural multi-host-multi-parasite community. Overall we will provide one of the most comprehensive views of how very different parasites, with different transmission modes, use multiple host species to persist, and the implications for how such parasites respond to targeted host treatment. Given the increasing concerns about emerging infectious diseases around the globe, it has never been more pressing to develop a genuine understanding of the factors affecting parasite invasion, transmission, persistence, and control. This project will be a major step in that direction.

As described in the 'Academic beneficiaries' section of this form, our primary beneficiaries will be the broad international scientific community working on infectious diseases. These academics, and wider collaborators, will directly benefit from the unique insights gained from this project, guiding current studies, and encouraging future research efforts that embrace the complexity of natural host-parasite communities. Impact with our primary beneficiaries, the academic community, will be initially through routine channels (peer reviewed publications (open access where possible), conference presentations, visits to other institutions and visits to our field sites). We will also initiate a Wiki-style online discussion resource, hosted through Liverpool University, enabling researchers from across the globe the chance to discuss relevant issues. In addition we will organise a 3-day workshop to explore practical aspects in the study of complex multi-host-multi-parasite communities, through a combination of presentations on key methodological topics (data analysis methods, mathematical modelling, ecological experimentation), discussion groups, and practical workshops in which participants will work through analyses of data in groups.

Other beneficiaries are future scientists. Throughout our existing NERC grant we have hired many undergraduate field assistants to help with the demanding trapping schedule and lab work of the project. These students have benefitted enormously from this experience, gaining expertise in the technical aspects of the project (field work, small mammal handling, lab assays and parasite identification) and, possibly more importantly, the whole process of research. Many of these students commented that it was the best thing they did at University, and they felt genuinely inspired by the experience. These students are now applying for graduate degrees in areas such as computational biology, veterinary parasitology and conservation, and we believe that their experience with us is crucial for their development as young scientists. We will do the same with this project, employing a number of undergraduate assistants (18) throughout its 3 years, and providing them with the opportunity to play a fundamental role in biological research. Furthermore, we will expand these volunteer opportunities to allow science teachers, school students (for example through the Nuffield bursary scheme) and other members of the public, to gain first-hand experience in cutting edge science, research methods, and practical field skills.

Finally, this project will also have relevance for non-academic beneficiaries, including conservation policy makers interested in the role that infectious diseases can have on threatened species, and those in the medical and veterinary communities where transmission of a pathogen from wildlife is of vital concern. Given our tractable field system, we have the ability to do field large-scale field manipulations, which are difficult to impossible in other mammal and human systems. These results can therefore provide general insight into identifying what data are needed to measure the contribution of each host species to disease persistence. Thus, this project has the potential to provide clear guidelines to public health and agricultural bodies into how to collect and analyse the appropriate data necessary to develop truly effective disease management programmes.

To engage with non-academics, we will post a regular blog on an established blogpage hosted by the owners of one of our field sites (http://www.woodlands.co.uk/blog/). We will provide regular updates of host species abundance patterns throughout the year, allowing the public to appreciate the hidden biodiversity within these woodlands, and get a feel for the kind of research that we do.