The impact of resource availability on parasite transmission: insights from a natural multi-parasite community

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

Abstract

Understanding the relationship between resource availability and parasitic infection in wildlife is of increasing importance given rising rates of habitat modification and anthropogenic change. These changes can alter the distribution, quality and availability of resources, either accidentally or deliberately. However, understanding how different resource availability scenarios, either natural or anthropogenic, affect infection levels in wildlife is a major conservation challenge due the myriad of ways in which resources affect hosts, both at the individual and population scales. Most studies into the relationship between resources and infectious disease focus only on specific aspects (e.g. how food quality affects host physiology, or how food levels affect host population size). In reality the impact of resources on the risk and burden of disease can be complex, affecting various aspects at both the individual and population levels. For example, high quality resources may significantly improve individual health and condition, resulting in reduced susceptibility to disease. However, aggregated food patches that attract groups of animals can lead to increased opportunities for parasite transmission. Importantly, the relative sizes of these effects are likely to differ for parasites with different transmission modes or lifecycles. Given these diverse effects, it can be highly challenging to understand and predict the impact of different resource availability scenarios in natural wildlife systems. This knowledge gap forms a major barrier to understanding how resources affect wildlife conservation and, for some diseases, human and domestic animal health.

To help understand the relationship between resource availability and wildlife disease we need to assess (1) different types of resource availability (e.g. aggregated v. evenly distributed, high v. low quality food), (2) the effects on different types of parasites (e.g. direct v. environmentally transmitted, chronic v. acute infections) and (3) whether those effects are due to changes in host physiology, behaviour, demography, or other parasites. To our knowledge, no studies have addressed all these aspects in the same study. However we have developed an ideal natural system: wild wood mice and their diverse parasite community. Not only have we optimised the methods for studying this host-parasite community in its natural setting, we have also recently developed a lab colony of formerly wild wood mice and some of their key natural parasite species, which provides unprecedented ability to combine intensive lab experiments with extensive field studies, using the same host-parasite community.

Here we will combine (1) lab studies of host and parasite responses to a range of infections/coinfections and resource availabilities, with (2) large-scale perturbation experiments using alternative resource provisioning scenarios in the wild to measure how different forms of resource availability affect transmission of a broad range of parasite types in their natural host. Furthermore, we will combine these results with general mathematical models of alternative resource scenarios to develop a broad understanding of how different resource-transmission relationships affect disease spread. Together, these approaches will allow us to: (1) assess how host physiology and behaviour change following alternative resource availability scenarios, (2) test whether we can make generalised predictions about how different parasites will respond to different types of resources, and (3) provide insight into how other wildlife systems are likely to respond to changes in resource availability scenarios in the future. Given increasing concerns over how anthropogenic activities impact wildlife, this project is highly timely, and will provide much-needed experimental data, and general insight, into how shifts in resource availability and distribution drive parasite dynamics in natural wildlife communities.

Planned Impact

Aside from the international scientific community working on infectious diseases, and broader issues of population and community ecology, this project will be of considerable relevance for non-academic beneficiaries. In particular it will be directly relevant to those working in the areas of conservation policy and wildlife management, who are interested in the effect of environmental or species-level perturbations (in particular food supplementation) on species contact networks, wildlife management and disease spread. Given our tractable field system, we have the ability to conduct large-scale field treatment experiments, which are difficult or impossible to conduct in other mammal (including human) systems. We have specifically chosen to focus on 'exemplar' groups of parasites that have characteristics that are representative of many parasites found in many natural systems. Thus, this project has the potential to provide broadly applicable guidelines to public health and agricultural bodies into the likely effects of different forms of resource provisioning on a wide range of parasite types. As ever we will publicise our work to non-academic audiences through press releases, science festivals (e.g. Edinburgh International Science Festival and University of Edinburgh Research Open Days), public engagement (Soapbox Science events (http://soapboxscience.org) blogs and podcasts (e.g., planetearth.nerc.ac.uk/multimedia/story.aspx?id=1623, Naturally Speaking https://naturallyspeakingpodcast.wordpress.com) and specialist publications (e.g., Fenton & Pedersen. 'Parasite diversity among wood mice and bank voles in the North West of England'. Mammal News, 2014).

Finally, as detailed further in the 'Academic Beneficiaries' section, other key beneficiaries will be the undergraduates that help on our project; not only those that go on to become the scientists of the future, but also those that don't go into science, but have an enhanced understanding of the practicalities of science. Our previous undergraduate field assistants (>60) benefitted enormously from the experience, and many commented that it was the best thing they did at University. In many cases this experience directly inspired them to go on to further scientific education and research (e.g., postgraduate education and training). Even for those that don't become scientists, they still gain invaluable experience in the scientific method and the practicalities of science, making them better-informed and more scientifically-aware citizens. We will employ a further 10 undergraduate assistants (plus a number of volunteer helpers) throughout this project, and will aim to give them the same experience as those previous assistants.
 
Description Gastrointestinal helminths are common parasites of humans, wildlife, and livestock, leading to chronic infections in large parts of the world. In humans, there is also an overlap in the incidence of malnutrition and helminth infections which can predispose individuals to higher infection burdens and reduced anthelmintic efficacy due to compromised immunity. This relationship has been well-studied in laboratory models by testing for the impact of dramatic reductions of specific macro- or micro-nutrients on infection outcomes. However, much less is known about the benefits of whole-diet supplementation in natural host-helminth systems. We experimentally supplemented the diet of wood mice (Apodemus sylvaticus) and measured anthelmintic treatment efficacy and resistance to the gastrointestinal nematode Heligmosomoides polygyrus in both natural and captive populations. In both settings, supplemented wood mice were more resistant to H. polygyrus infection, cleared worms more efficiently after treatment, had better body condition, and higher general and parasite-specific immune responses. In addition, supplemented nutrition in conjunction with anthelminthic treatment significantly reduced H. polygyrus transmission. These large-scale improvements in condition and immunity of supplemented nutrition found in controlled and wild environments show the rapid benefits of a well-balanced diet and have important implications for using diet interventions to improve disease control programmes. We have found that both the quality of food supplementation and the way the food is distributed (either evenly spread or aggregated in a central feeder) can have significant impacts on all types of parasites and pathogens; with some increasing, while the burden of other parasites goes down. We also found that mice move very different when food is readily available, and this may be having an impact on the spread of parasites and pathogens.
Exploitation Route We have begun to publish results from this work, the results of which have highlighted the large effect that supplemental resources can have on both hosts and their parasites and pathogens. While we are continuing to analyse the data and will publish further outcomes, we believe that our results will better help understand heterogeneities in drug treatment successful and infection burdens and the impact of anthropogenic food on the host-parasite interactions of wildlife.
Sectors Agriculture, Food and Drink,Environment

 
Description A new 'lab-to-wild' model for investigating the impact of natural gut microbiota on immunity, infection and health
Amount £22,980 (GBP)
Funding ID 1107 
Organisation Royal Society of Edinburgh (RSE) 
Sector Charity/Non Profit
Country United Kingdom
Start 06/2021 
End 11/2021
 
Description A simple epigenetic clock for a wild mouse'
Amount £7,724 (GBP)
Organisation Wellcome Trust 
Department Wellcome Trust Institutional Strategic Support Fund
Sector Charity/Non Profit
Country United Kingdom
Start 01/2019 
End 12/2019
 
Description Royal Society Newton International Fellowship to Camille Jacqueline - 'The role of microbiota in ageing and cancer: a mosaic tissue perspective'
Amount £67,000 (GBP)
Organisation The Royal Society 
Sector Charity/Non Profit
Country United Kingdom
Start 07/2021 
End 07/2023
 
Description Testing the real-world efficacy of a novel anthelmintic vaccine based on targeting RNA transmission'
Amount £21,239 (GBP)
Funding ID IS3-R3.18 21/22 
Organisation Wellcome Trust 
Department Wellcome Trust Institutional Strategic Support Fund
Sector Charity/Non Profit
Country United Kingdom
Start 02/2022 
End 12/2022
 
Description The ecology within: the impact of gut ecosystem dynamics on host fitness in the wild
Amount £3,570,094 (GBP)
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 03/2019 
End 02/2025
 
Description The evolution of RNA transmission between animals in the wild
Amount £185,990 (GBP)
Organisation The Leverhulme Trust 
Sector Charity/Non Profit
Country United Kingdom
Start 07/2020 
End 06/2022
 
Description Understanding within-host helminth-microparasite interactions and predicting population- level outcomes
Amount £12,000 (GBP)
Organisation The Royal Society 
Sector Charity/Non Profit
Country United Kingdom
Start 03/2020 
End 03/2022
 
Title Collection of biological samples from wild wood mice 
Description Over the course of our 3 years of field work on this grant, we collected >1800 faecal samples and >1200 blood samples from known wild wood mice. From these samples we are using a series of diagnostic tests to identify host factors (i.e. antibodies, stress hormones, leptin, protein, etc) and infection status with a suite of gastrointestinal parasites and pathogens. This data set will be available to the biological community once it is completed. 
Type Of Material Biological samples 
Year Produced 2021 
Provided To Others? No  
Impact This set of biological will be used to address the key question proposed by this grant - but in addition it can be used by other groups to test for confection interactions. 
 
Title Creation of an epigenetic clock to age wild wood mice 
Description We used patterns of methylation to create an epigenetic clock that can age wild wood mice within 21 days of their birth. This novel method is very important for enhancing our understanding of health ageing and has not been done in wild mice before. 
Type Of Material Model of mechanisms or symptoms - mammalian in vivo 
Year Produced 2020 
Provided To Others? No  
Impact We will be publishing this result and making the methods, techniques and bioinformatics pipeline freely available in 2020. 
 
Title Wild derived parasite isolates 
Description We have collected wild isolates of several important murine pathogens and parasites that can then be used in laboratory experiments to test natural host - parasite combinations. 
Type Of Material Model of mechanisms or symptoms - non-mammalian in vivo 
Year Produced 2019 
Provided To Others? Yes  
Impact These wild derived parasites have been a part of a recently published paper (Clerc et al. 2019), contributed to the preliminary data that was used in a successful NERC Standard Grant application (2018) and will be shared with other groups working on these systems. 
 
Title RFID Movement Logger Data for Wild Mice 
Description We have been following individually tagged wood mice in three populations, based on a RFID stationary logger systems - across different nutritional supplemention experiments. This data set includes specific spatial location for >100 wood mice across 24 months - totally hundreds of thousands of datapoint. 
Type Of Material Database/Collection of data 
Year Produced 2021 
Provided To Others? No  
Impact We are currently using this data set within this grant, after which it will be publicly available. 
 
Description Participation in an activity, workshop or similar - Edinburgh International Science Festival 2019 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Public/other audiences
Results and Impact Several members of the Pedersen research group constructed an activity and booth for the Edinburgh International Science Foundation about host-parasite interactions and then presented this activity to children over the course of several days.
Year(s) Of Engagement Activity 2019