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

Lead Research Organisation: University of Edinburgh
Department Name: Sch of Biological Sciences

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
 
Title Age specific impacts of vegetation functional traits on gastro-intestinal nematode parasite burdens in a large herbivore 
Description Gastro-intestinal nematode (GIN) parasites play an important role in the ecological dynamics of many animal populations. Recent studies suggest fine-scale spatial variation in GIN infection dynamics is important in wildlife systems, but the environmental drivers underlying this variation remain poorly understood. We used data from over two decades of GIN parasite egg counts, host space use, and spatial vegetation data from a long-term study of Soay sheep on St Kilda to test how spatial autocorrelation and vegetation in an individual's home range predict parasite burden across three age groups. We developed a novel approach to quantify the plant functional traits present in a home range to describe the quality of vegetation present. Effects of space and vegetation varied between age classes. In immature lambs, strongyle parasite faecal egg counts (FEC) were spatially structured, being highest in the north and south of our study area. Independent of host body weight and spatial autocorrelation, plant functional traits predicted parasite egg counts. Higher egg counts were associated with more digestible and preferred plant functional traits, suggesting the association could be driven by host density and habitat preference. In contrast, we found no evidence that parasite FEC were related to plant functional traits in the host home range in yearlings or adult sheep. Adult FEC were spatially structured, with highest burdens in the north-east of our study area, while yearling FEC showed no evidence of spatial structuring. Our findings support the importance of fine-scale environmental variation for wildlife disease ecology and provide new evidence that such effects may vary across demographic groups within a population. Parasite burdens in immature individuals appear more readily influenced by fine-scale spatial variation in the environment, highlighting the importance of such heterogeneity for our understanding of wildlife epidemiology and health. 
Type Of Material Database/Collection of data 
Year Produced 2023 
Provided To Others? Yes  
URL https://datadryad.org/stash/dataset/doi:10.5061/dryad.z08kprrjf
 
Title Correlates of early reproduction and apparent fitness consequences in male Soay sheep 
Description Life history trade-offs are ubiquitous across species and place constraints on the timing of life history events, including the optimal age at first reproduction. However, studies on lifetime breeding success of male mammals are rare due to sex-biased dispersal and the requirement for genetic paternity inferences. We studied the correlates and apparent fitness consequences of early-life reproduction among males in a free-living population of Soay sheep (Ovis aries) on St Kilda, Scotland. We investigated the factors associated with early breeding success and the apparent consequences of early success for survival and future reproduction. We used genetic paternity inferences, population data and individual morphology measurements collected over 30 years. We found that individuals born in years with low-density population size had the highest early-life breeding success, and singletons were more likely to be successful than twins. Individuals that bred successfully at seven months were more likely to survive their first winter. For individuals that survived their first winter, early breeding success was not associated with later breeding success. Since individual heterogeneity affects breeding success, we believe that variation in individual quality masks costs of early reproduction in this population. Our findings provide no evidence for selection for delayed age at reproduction in male Soay sheep. 
Type Of Material Database/Collection of data 
Year Produced 2023 
Provided To Others? Yes  
URL http://datadryad.org/stash/dataset/doi:10.5061/dryad.wm37pvmsh
 
Title On-line tutorial to support use of novel method to analyses gut microbiome data 
Description On-line tutorial to support novel, mixed-effects model approach to analyse gut microbiome data. This is in support of recent publication of methodology in journal mSystems. 
Type Of Technology New/Improved Technique/Technology 
Year Produced 2023 
Impact None as yet. 
URL https://arsweeny.github.io/microbiome-glmm/
 
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 164 followers (5th March 2021).
Year(s) Of Engagement Activity 2019
URL http://soaysheep.biology.ed.ac.uk/ecologywithin
 
Description Leaflet on Soay sheep research project 
Form Of Engagement Activity A magazine, newsletter or online publication
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Public/other audiences
Results and Impact Produce and disseminated an informational leaflet for general public visiting St Kilda (>2,000 visitors per year) about our research project. First run of 500 leaflets were handed out by ourselves and island's owners (National Trust for Scotland) very rapidly and we have produced further 500 leaflets. Feedback on these has been very positive.
Year(s) Of Engagement Activity 2023,2024
 
Description Moredun Magazine article 
Form Of Engagement Activity A magazine, newsletter or online publication
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Industry/Business
Results and Impact Moredun Magazine, Issue 17 Article: "The quest to know Soay sheep inside out!" by Tom McNeilly et al.
Year(s) Of Engagement Activity 2019
URL https://www.moredun.org.uk/publications/moredun-magazine
 
Description Press Release by Aberystwyth University 
Form Of Engagement Activity A press release, press conference or response to a media enquiry/interview
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Public/other audiences
Results and Impact Press release regarding setting up of experimental flock of Soay sheep.
Year(s) Of Engagement Activity 2019
URL https://www.aber.ac.uk/en/news/archive/2019/06/title-223707-en.html
 
Description STEM Village Webinar 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Postgraduate students
Results and Impact Outreach presenting research to broad audience & highlighting LGBTQ+ researchers - talk given by project post-doc doc, Amy Sweeny, entitled: "Harnessing the complexity of wild populations: what can diversity teach us about disease?"
Year(s) Of Engagement Activity 2020
 
Description Stakeholder engagement - Feb 2020 
Form Of Engagement Activity A formal working group, expert panel or dialogue
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Industry/Business
Results and Impact Presentation to NFU Cymru President, Chair and senior Policy Advisors regarding on-going and future research that will support a transition to net zero farming by 2040.
Year(s) Of Engagement Activity 2020
 
Description WWF Earth Hour twitter post from St Kilda 
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 Twitter broadcast from St Kilda on project Twitter feed in support of WWF's Earth Hour project
Year(s) Of Engagement Activity 2020