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

Lead Research Organisation: Moredun Research Institute
Department Name: Disease Control

Abstract

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.

Planned Impact

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.

Publications

10 25 50
 
Description We have identified key types of immune response which are associated with resistance to parasites in sheep. Importantly the two types of parasites which infect the Soay sheep on St Kilda seem to be controlled by different types of immune response, and that sheep appear to be able to generate these different immune response at the same time to simulataneously control both types of parasite.
We have also developed methods to simultaneously characterise the type of bacteria (microbiome) and types of worm parasites (nemabiome) present in sheep faeces. These will be used to determine how the nemabiome, microbiome and immune response interact, and what the consequences are for fitness and survival of wild mammals.
Exploitation Route The results from the immunological analysis are of direct relevance to sheep farmers (and other livestock producers) who are interested in selectively breeding for animals with increased parasite resistance.
Nemabiome technology can also be applied to farmed livestock to assist in developing parasite control strategies, including identifing drug-resistant parasite species and differentiating between disease causing and non-disease causing parasites.
The outputs of this project may also be useful for human studies exploring the link between the gut microbiome, immunity and health.
Sectors Agriculture, Food and Drink,Healthcare

 
Title High-throughput T cell phenotyping in wild mammal populations 
Description A method has been developed to allow high-throughput phenotypic analysis of circulating T cells within wild sheep. The method uses a combination of flow cytometry and cytokine release assays to define key transcription factors and cytokine profiles associated with different types of T-helper (Th) cells (T-helper type 1 (Th1), Th2, Th17 and Treg) within an individual blood sample. 
Type Of Material Physiological assessment or outcome measure 
Year Produced 2019 
Provided To Others? No  
Impact Use of this research method has allowed us to identify associations between different T-helper cell profiles and parasite infections in the wild. 
 
Title Nemabiome sequencing in sheep 
Description A protocol has been developed and optimised in which next generation sequencing is used to determine the composition of different nematode species in ovine faecal samples. 
Type Of Material Technology assay or reagent 
Year Produced 2020 
Provided To Others? Yes  
Impact This methodology is currently being used in the ECOWI project and the methods will be made publically available for other research groups. 
 
Title Ovine IgG subclass-specific ELISA 
Description Monoclonal antibody reagents have been generated to evaluate IgG1 and IgG2 responses to parasite infections in sheep. 
Type Of Material Technology assay or reagent 
Year Produced 2020 
Provided To Others? Yes  
Impact Multiple requests for the monoclonal antibodies whcih have been distributed to other laboratories together with the ELISA protocol. 
 
Title Ecology Within Immune Phenotype database 
Description A database has been generated of blood immune profiles (numbers of circulating CD4 and CD8 cells, T-helper transcription factor expression data, cytokine release assay data) from ~200 individual Soay sheep. 
Type Of Material Database/Collection of data 
Year Produced 2019 
Provided To Others? No  
Impact This database has been used to identify associations between T-helper cell immune profiles and levels of gastro-intestinal parasite infection. 
 
Description Earth Hour Twittter post from St Kilda 
Organisation World Wide Fund for Nature
Country Switzerland 
Sector Charity/Non Profit 
PI Contribution Earth Hour Twittter post from St Kilda
Collaborator Contribution Branded material and event information
Impact Twitter post.
Start Year 2020
 
Description Earth Hour Twittter post from St Kilda 
Organisation World Wide Fund for Nature
Country Switzerland 
Sector Charity/Non Profit 
PI Contribution Earth Hour Twittter post from St Kilda
Collaborator Contribution Branded material and event information
Impact Twitter post.
Start Year 2020
 
Description The Environmental Engagement Training Academy training event 
Organisation Association for Science and Discovery Centres
Country United Kingdom 
Sector Charity/Non Profit 
PI Contribution Attendance and discussion during training event.
Collaborator Contribution Delivery of the Operation Earth Training Academy
Impact Further discussion on the project by attendees of the training academy (children/families).
Start Year 2021
 
Description Understanding coccidian species diversity in the St. Kilda Soay sheep population 
Organisation University of Las Palmas de Gran Canaria
Country Spain 
Sector Academic/University 
PI Contribution Coccidian parasites affecting sheep include multiple different species of Eimeria, which are currently identified by the characteristic morphology of their eggs (oocysts) (also referred to as the 'morphospecies'). This, however, is a specialist skill. At Moredun we have generated oocysts from a number of individual Soay sheep faecal samples and sent this to our collaborators for speciation.We have also hosted a member of our collaborator's research team at Moredun to establish the speciation methodology at Moredun.
Collaborator Contribution Our partners have performed speciation of Eimeria oocysts from a range of individual sheep, and provided training in Eimeria morphospeciation to staff at Moredun.
Impact This collaboration has provided information on Eimeria species within the St Kilda Soay sheep population. This collaboration will be part of a future multi-disciplinary approach involving experts in protozoan genomics in which Eimeria species information will be compared with Eimeria genomic sequencing data to develop molecular tools capable of identifying different Eimeria genotypes/species within individual sheep faecal samples.
Start Year 2019
 
Description An ecologist's adventures in livestock disease (Cardiff University) 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Postgraduate students
Results and Impact Scientific presentation on eco-immunology and the wider Ecology Within project.
Year(s) Of Engagement Activity 2019
 
Description An ecologist's adventures in livestock disease (Moredun group seminar series) 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Professional Practitioners
Results and Impact Scientific presentation on eco-immunology and the wider Ecology Within project.
Year(s) Of Engagement Activity 2019
 
Description Ecology Within website & twitter feed 
Form Of Engagement Activity Engagement focused website, blog or social media channel
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact Published project website outlining the project's aims & team members - http://soaysheep.biology.ed.ac.uk/ecologywithin - aimed at general audience And simultaneously launched Twitter feed (@soayecowithin) to publicise events and activities including fieldwork. lab work, publications, meetings, and talks. Currently has 147 followers (2nd March 2020).
Year(s) Of Engagement Activity 2019
URL http://soaysheep.biology.ed.ac.uk/ecologywithin
 
Description Glasgow University Pride & Outreach event (Talk: Harnessing the complexity of wild populations: what can diversity teach us about disease?) 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact Glasgow University Pride & Outreach event highlighting LGBTQ+ Scientists promoting discussion.
Year(s) Of Engagement Activity 2020
 
Description Good Faith Idea Exchange Podcast 
Form Of Engagement Activity A broadcast e.g. TV/radio/film/podcast (other than news/press)
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact Spotify podcast interview to talk about the EcoWithin project and careers in science and conservation
Year(s) Of Engagement Activity 2021
 
Description Invited presentation: Exploring defence against infection in the sheep at the edge of the world 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Postgraduate students
Results and Impact An invited presentation was delivered to staff and students at the University of Calgary on the use of Soay sheep to understand immunity in wild mamal systems. The talk generated discussion around the St Kilda Soay project and the causes of immune variation in outbred populations.
Year(s) Of Engagement Activity 2020
 
Description Moredun Research Institute seminiar: From Field to Lab, a tale of sheep and cells 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Postgraduate students
Results and Impact An institute seminar was given on the project to students and staff of the Moredun group and associated organisations. The talk focused on immunity to parasites and how to quantify this in wild ruminants. The talk stimulated questions around both the project and the methodology and led to discussion on how to apply these methods to farmed livestock.
Year(s) Of Engagement Activity 2021
 
Description Presentation to Danish Sheep Vet group (Team Fareradgivning) on control of gastro-intestinal parasites in sheep 
Form Of Engagement Activity A formal working group, expert panel or dialogue
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact The purpose of this engagement activity was to provide expert advice to a working group of Danish Sheep Veterinarians on control of gastro-intestinal parasites in sheep. This included detailed discussions on the immunological basis of parasite resistance in sheep and how nematode species information can be used to inform parasite control strategies.
Year(s) Of Engagement Activity 2019
 
Description STEM Village Webinar (Talk: Harnessing the complexity of wild populations: what can diversity teach us about disease?) 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact Outreach presenting research to broad audience & highlighting LGBTQ+ researchers
Year(s) Of Engagement Activity 2020
 
Description The quest to know Soay sheep inside out! 
Form Of Engagement Activity A magazine, newsletter or online publication
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Professional Practitioners
Results and Impact Article in Moredun Spring/Summer Magazine on the Ecology Within project which is sent to the Moredun Foundation members (~13,000 individuals). The article gave an overview of the project and stimulated discussions with our membership (farmers, vets, government and industry representatives, members of the public) at internal and external stakehoder events.
Year(s) Of Engagement Activity 2019
URL https://www.moredun.org.uk/publications/moredun-magazine