Pemberton, Josephine

Nussey, Daniel

Albery, Gregory

Natural Environment Research Council (NERC)

2020-02-05T12:43:17Z

2020-02-05T12:43:17Z

2020-01-06

Parasites are a ubiquitous presence in nature that can profoundly impact the evolution and ecology of their hosts. Despite their longstanding interest for many branches of mammalian biology, there are relatively few large-scale longitudinal investigations of immunity and parasitism in large wild mammals. Furthermore, very few studies take full advantage of longitudinal studies’ ability to examine spatiotemporal variation, life history correlates, and fitness consequences of immunity and parasitism simultaneously. This thesis comprises the first parasitological and immunological investigation in the individually-monitored study population of red deer (Cervus elaphus) on the Isle of Rum in the Inner Hebrides, Scotland. Over the course of nine field seasons spanning 2016-2018, colleagues and I collected 2091 faecal samples from 447 identified individuals. I examined these faecal samples for eggs and larvae of gastrointestinal helminth parasites and protozoa. I particularly focussed on counts of three highly prevalent helminth taxa: strongyle nematodes, the common liver fluke Fasciola hepatica, and the tissue nematode Elaphostrongylus cervi. In addition, I adapted and employed a method of faecal antibody quantification originally developed for use in sheep. Samples were analysed for total immunoglobulin A (IgA) and anti- Teladorsagia circumcincta-specific IgA, giving measures of both general and specific immune allocation. I used these immune and parasite measures in several analyses, making use of the high-resolution life history, fitness, and behavioural data available for the Rum red deer population, focussing mainly on samples collected from adult females. The principal findings were: 1. The red deer were infected with multiple species of helminths and protozoa, present at high prevalence but relatively low intensity. These parasites showed seasonal patterns of infection with strong age and sex biases, all of which varied between parasite taxa. Generally, younger individuals had higher helminth intensities, and autumn and winter seasons featured the lowest parasite intensities. 2. Parasite counts were repeatable within individuals. However, repeatability varied according to the sampling timescale, with strongyle counts being more similar within sampling trips than between trips. This implied contrasting seasonal patterns in different individuals, so that sampling at different times of year would give different impressions of patterns of parasitism across the population. 3. Females that reproduced had lower antibody levels and higher parasite intensities in the following year. However, different components of reproduction had different costs for different immune and parasite measures: gestation was associated with lower total IgA levels, while only lactation resulted in increased parasite counts, implying an important role of exposure in mediating reproduction-parasitism tradeoffs in this system. 4. I investigated the impact of reproduction, immunity, and parasitism on fitness-related traits using path analysis. Parasite count in a given year was found to correlate negatively with reproduction the following year, indicating a possible cost of parasitism for multiple fitness-related traits, above and beyond that accounted for by current reproductive status itself. Increased anti-Teladorsagia circumcincta IgA was also found to be associated with increased probability of reproduction, beyond any association with strongyles themselves. 5. I quantified and controlled for spatial patterns of immunity and parasitism using Integrated Nested Laplace Approximation (INLA) models. These analyses revealed stark differences in the range and patterns of spatial heterogeneity for different immune and parasite measures. However, fixed effects remained largely unchanged by the incorporation of spatial effects, indicating that spatial variation was unlikely to be confounding my earlier findings. I discuss these findings and their implications for longitudinal studies of immunity and parasitism in wild animals and the further integration of spatiotemporal, life history, immune, and parasite data.

https://hdl.handle.net/1842/36744

http://dx.doi.org/10.7488/era/51

en

The University of Edinburgh

Albery GF, Kenyon F, Morris A, Morris S, Nussey DH, Pemberton JM (2018). Seasonality of helminth infection in wild red deer varies between individuals and between parasite taxa. Parasitology 145, 1410–1420. https://doi.org/10.1017/S0031182018000185

Albery, G. F., Watt, K., Keith, R., Morris, S., Morris, A., Kenyon, F., Nussey, D. H. and Pemberton, J. M. (2019). Reproduction has different costs for immunity and parasitism in a wild mammal. Functional Ecology. https://doi.org/10.1111/1365- 2435.13475

Albery GF, Nussey DH, Pemberton JM: Fitness costs of parasites explain multiple life history tradeoffs in a wild mammal. Preprint: https://www.biorxiv.org/content/10.1101/683094v1

Albery GF, Becker DJ, Kenyon F, Nussey DH, Pemberton JM (2019). The fine-scale landscape of immunity and parasitism in a wild ungulate population. Integrative and Comparative Biology, icz016, https://doi.org/10.1093/icb/icz016

wild red deer

Cervus elaphus

Isle of Rum

parasitic helminths

immune system

antibody levels

Fasciola hepatica

Elaphostrongylus cervi

immunoglobulin A

Integrated Nested Laplace Approximation

longitudinal study

Spatiotemporal and individual drivers of variation in parasitism and immunity in wild red deer

Thesis or Dissertation

Doctoral

PhD Doctor of Philosophy