IAP-24-086

Novel insights into tick-borne disease ecology through host blood meal identification

Ticks are important vectors of diseases. Tick species transmitting pathogens of concern tend to be host generalists, meaning they can feed on a wide range of vertebrate hosts. However, only some of these host species will act as infection reservoirs from which the tick can pick up the pathogen while feeding, to then pass it on during a subsequent blood meal (which could be a human host). For Lyme disease for example, ticks acquire the pathogen as larvae when feeding on competent hosts such as small mammals or birds (in contrast to non-competent hosts such as deer). The prevalence of the pathogen in ticks (affecting human infection risk), therefore depends on which host species ticks tend to feed on as larvae, which in turn will depend on the composition of the host community available to ticks to feed on. Being able to determine the source of larval blood meals thus offers powerful insights about the key host species contributing to transmission cycles and can help to explain and predict landscape-scale variation in tick-borne disease risk. New genetic methods for identifying tick blood meals have recently been developed in North America but remain so far under-explored for the main European tick vector, Ixodes ricinus. The project would combine method development with empirical tests based on a large collection of tick DNA samples from UK sites and mathematical models to gain novel insights into tick-borne disease dynamics in the UK.

Over the past decades, sensitive PCR-based methods have been applied to the host identification from tick blood meals with variable success. Early approaches suffered from low success rates (<30%) and low reproducibility. In contrast, a recently introduced qPCR approach based on the amplification of host-specific retrotransposons, occurring at high abundance within the host genome, has achieved detection success of 50-100% (Goethert et al. 2021), and has now been applied with similar success by multiple research groups (e.g. Tufts et al, 2024; Sormunen et al. 2024). However, applications of the retrotransposon-based approach to date have been limited to North American ticks and their hosts, apart from recent work in Finland (Sormunen et al. 2024). There is therefore much untapped potential to uncover the ecology of ticks and tick-borne pathogens in Europe, including the identification of reservoir hosts and the role of host community composition in tick-borne disease emergence. This project will fill this gap through a series of interlinked research objectives:
1) To design and validate primers and protocols for the detection of relevant vertebrate hosts in UK ecosystems
2) To apply this method to existing collections of DNA from field-collected ticks with known infection status for the Lyme disease pathogen Borrelia burgdorferi s.l., (Bbsl) starting with simple, species-poor host communities on islands (Millins et al. 2021) before moving to more diverse host communities from the UK mainland.
3) To use the empirical data from these systems to parameterise next-generation matrix models of tick populations and tick-borne pathogens (Hartemink et al. 2008) to gain a quantitative understanding of the contribution different vertebrate species make to Bbsl transmission and to predict the effect of host community changes, for example due to environmental gradients or targeted interventions, on infection rates

Year 1

Design and validate the first set of species-specific qPCR primers targeting samples a small set of potential vertebrate hosts (including samples for where host is known) for a species-poor island system on the Scottish Western Isles where Lyme disease has emerged recently (Millins et al. 2021) and for which we hold large collections of tick samples previously tested for Bbsl. Combine host identification results with mathematical models to identify infection reservoir and to explain spatial variation in pathogen prevalence.

Year 2

Write up empirical study from year 1 and share results with end users on the Western Isles. Expand qPCR primer set to include larger range of potential vertebrate host species from UK forest sites. Tick DNA collections and Bbsl infection data are available from 30 sites that were sampled for multiple years and for which host communities are well characterised (e.g. from camera trap data). Combine host identification data for ticks from these sites with mathematical models to test whether among site variation in Bbsl prevalence can be predicted as a function of tick host use.

Year 3

Write up empirical study from year 2 and share with stakeholders. Carry out additional empirical study using the host identification approach to examine relationships between host community composition and tick-borne pathogen prevalence in UK ecosystems. This could be done based on existing samples or through own sample collections. Alternatively, year 3 could be used for advancing and contrasting new methods for host blood meal identification or for trialling their application to non-European tick species.

Year 3.5

Write up results of studies from year 3. Complete thesis writing.

The project will provide a broad range of technical and transferrable skills including in molecular biology (e.g. primer design, qPCR), population modelling, vector ecology, data handling and analysis, and statistical inference. Training will be provided by the whole supervisor team. In addition to the University of Glasgow, where the molecular work and a large part of the analysis will be carried out, the student will have the opportunity to spend time at the Centre for Ecology and Hydrology, where Purse and White are based, to undergo training in population modelling of ticks and tick-borne pathogens.