The ecology within: The impact of gut ecosystem dynamics on host fitness in the wild

Individual animals are typically home to a staggeringly complex community of smaller organisms. This observation has led researchers to consider individuals as ecosystems in their own right, challenging us to think in new ways about how ecological processes may drive variation in an individual's health and fitness. The gut is rapidly emerging as an important example of how such within-individual ecosystems might interface with host physiology and health. In vertebrates, the gut is home not only to trillions of 'friendly' bacteria (the 'microbiota'), which have an essential role in extracting nutrition from food consumed, but also to diverse communities of parasites, which compete with their host for resources and can cause serious illness. The potential significance of this gut ecosystem for our understanding of the ecological and evolutionary dynamics of wild animal populations is immense. However, our current understanding of the drivers of gut ecosystem dynamics and their consequences for host fitness in natural populations is very limited.

The application of new next-generation sequencing methods to faecal samples represents a potentially transformative approach to non-invasively monitor gut community dynamics and diet in wild animals. This approach has already revolutionised our understanding of the human gut bacteria community and its role in health and disease, but has yet to be applied to wild study systems in which individual genotype, diet, immunity and fitness are all closely monitored. This project will apply this approach to faecal samples collected longitudinally from an exceptionally well-studied wild mammal population to simultaneously monitor variation in gut bacteria, protozoan and nematode communities and diet. This will allow us to address fundamental outstanding questions about which factors drive gut community dynamics within individuals and the outcomes of these dynamics for health and fitness under natural conditions. Our study system, the Soay sheep of St Kilda, will allow us to regularly and repeatedly sample known individuals with well-characterised genetics, environmental experiences and reproductive history. Our project will also involve the development and application of a novel statistical approach to integrate data on gut community ecology with our understanding of host ecology and genetics, and new ecological and epidemiological models that will transform our understanding of how the gut ecosystem impacts on host population and disease dynamics in nature.

Our project will provide the first integrated study mapping the relationships between gut commensal and parasite communities, host diet, immunity and fitness in the wild. Our findings will profoundly improve our understanding of the significance of within-host ecosystem across a broad range of ecological disciplines within NERC's remit, including population, community, disease and evolutionary ecology.

We have identified three major non-academic impact groups, and detail how our work will impact each below:

Conservation managers: We anticipate significant impacts for in- and ex-situ conservation management. We will be developing methods to monitor diet and gut community structure from faecal samples, and new techniques to analyse the data produced. Wildlife and conservation managers often need to know what particular groups and individuals are eating (e.g. to understand diet preferences in threatened species), how gut health and community structure of differs between wild and captive individuals (e.g. reintroduction programs), and the nature and degree of parasite transmission to threatened wildlife species (e.g. from livestock). Our project can provide readily useable and transferable protocols, tutorials and academic support in all these areas, offering more affordable and flexible methods and allowing conservation organisations to reduce reliance on commercial kits or services. Not only will this save them money, but it will crucially increase capacity to perform monitoring in developing countries, where sample transfer is difficult for legislative or political reasons. We believe this impact will be broad and of interest to major international conservation organisations and their members, including the World Association for Zoos and Aquariums and IUCN Specialist Groups (e.g. Reintroduction and Conservation Breeding groups).

Livestock industry & agricultural policy makers: In the UK, gastro-intestinal nematode infections cost the livestock farming industry an estimated £80 million annually, whilst Eimeria infections result in an estimated 6-9% gross margin reduction. Resistance to available anthelminthic drugs is emerging rapidly and is a major current concern for the industry and policy makers. The non-invasive monitoring methods we will develop could be applied in agriculture to monitor changes in gut parasite communities after drug treatment to better understand the consequences for different worm and Eimeria species and improve targeting of treatment. Furthermore, the epidemiological models we will develop can help identify optimal strategies to reduce anthelmintic treatment, and will offer a platform for the development of evolutionary models of nematode drug resistance to help limit its spread. Additionally, intensive approaches to livestock farming on grasslands, which make up two-thirds of UK agricultural land, are increasingly uneconomic and there is growing need to optimise livestock stocking densities and diversity. The flora of St Kilda is typical of many hill and upland sheep farming sites in the UK and our project will provide valuable new understanding of how natural sheep grazing preferences change in the light of age, season, parasite load and climatic conditions. The application of this knowledge and of models to describe these behaviours will enable predictive anticipation of the optimal grazing regimes needed to meet the ever-changing needs of the market and of policy priorities.

General public: There is rapidly growing public and media interest in the role the gut microbiota plays in human health (e.g. recent coverage in Vogue magazine, and BBC's "Trust me, I'm a doctor" series). There is also considerable public interest in the remarkable natural history of St Kilda (e.g. a feature in latest series of BBC's "Coast" and coverage of the Soay sheep project's research in The Sun, BBC news and many others). This is coupled with a recent increase in accessibility of St Kilda to the general public: there are currently five boat tour operators based in the Outer Hebrides bringing >5,000 tourists ashore each year. By engaging with the media, general public and visitors to St Kilda about our work, we will enhance public understanding of the role of gut ecosystems in human and animal health, as well as the importance of basic ecological principles for our understanding of wild animal populations.