Biology subjects

Sweeny, A. R.

Publications and source records attributed to Sweeny, A. R..

16 recordsLinked to original sources

bioRxiv2026

Fitness costs of parasitism depend on fine-scale density and resource availability in a wild ungulate

Resource competition and parasite exposure both present common density-dependent fitness costs for wild animals. Because launching effective immune responses is costly in terms of resources, parasites fitness costs should be further exacerbated in high-density, resource-depleted areas. To disentangle these relationships, we related density, parasitism, and resource availability to survival and fecundity across lifespan in a long-term study of wild red deer. All fitness measures declined with a combination of parasite count, greater density, and reduced resource availability. Beyond these relationships, as expected, local density and resource scarcity exacerbated survival costs of parasitism in calves, effectively undermining tolerance of infection. However, these synergistic relationships faded in yearlings and then reversed in adults, likely through age-structured selection biases. These findings emphasize that the costs of parasites and resource scarcity can be synergistic and intertwined with density in wild populations, accentuating the value of incorporating resource competition when examining parasite-dependent population regulation.

ecology↗

bioRxiv2025

Resource supplementation alters host exposure, susceptibility, and infection dynamics across a diverse parasite community

Resource availability is crucial in shaping exposure and resistance to parasites. Although effects are expected to vary across parasite species, most of our knowledge comes from single-host, single-parasite studies. In a wild wood mouse population (Apodemus sylvaticus), we supplemented dietary resources over 3 years and quantified effects on a diverse parasite community alongside host behaviour and physiology. Resource supplementation had diverse impacts on 12 parasite taxa including positive (3/12), negative (6/12), and null (3/12) results. Supplementation also influenced host biology, with supplemented mice moving less, experiencing higher conspecific densities, improved conditions, and increased reproduction. These findings experimentally demonstrate that resource availability can multifacetedly affect disease dynamics. The complexity likely arises due to combined effects on exposure and susceptibility processes. Our study advances understanding of disease drivers at the human-wild interface and underscores the importance of assessing whole parasite communities to predict responses to changing resource landscapes in the wild.

ecology↗

bioRxiv2025

The macroecology of viral coinfection

Coinfection is common in wild animals, and can profoundly influence disease outcomes and transmission. However, most coinfection research is based on laboratory experiments or a few well-studied wildlife systems. Here, we use data from the PREDICT project - the largest standardized wildlife disease surveillance project ever conducted - to describe patterns of viral coinfection and evaluate their association with host and virus factors. Within the viruses prioritized for testing, we find that coinfection is rare (detected in just 223 of 65,662 animals), but still more common than expected by chance - especially coinfections of coronaviruses, paramyxoviruses, and influenza A virus. We further find that coinfection is associated with host age, but bats and rodents exhibit opposing relationships. We find that captive wild animals (specifically rats and mallards) exhibit higher coinfection than free-ranging wild animals, highlighting potential risks to wildlife and human health from the wildlife trade. Finally, we find that biases in sampling and testing can shape observed patterns of coinfection. Our results characterize associations among viruses in the largest relevant dataset currently available. Factors associated with coinfection in this dataset such as host-level variation, virus-virus interactions, and human interference should be further tested via surveillance and laboratory approaches to better resolve the role of coinfection as an important and likely overlooked driver of viral dynamics in nature.

ecology↗

bioRxiv2024

Density-dependent network structuring within and across wild animal systems

High population density should drive individuals to more frequently share space and interact, producing better-connected spatial and social networks [1-4]. Although this theory is fundamental to our understanding of disease dynamics [2,5-8], it remains unconfirmed how local density generally drives individuals positions within their networks, which reduces our ability to understand and predict density-dependent processes [4,9,10]. Here we provide the first general evidence that density drives greater network connectedness at fine spatiotemporal scales, at the scale of individuals within wild animal populations. We analysed 36 datasets of simultaneous spatial and social behaviour in >58,000 individual animals, spanning 30 species of fish, reptiles, birds, mammals, and insects. 80% of systems exhibited strong positive relationships between local density and network centrality. However, >80% of relationships were nonlinear and 75% became shallower at higher values, signifying that demographic and behavioural processes counteract densitys effects, thereby producing saturating trends [11-15]. Densitys effect was much stronger and less saturating for spatial than social networks, such that individuals become disproportionately spatially connected rather than socially at higher densities. Consequently, ecological processes that depend on spatial connections (e.g. indirect pathogen transmission, resource competition, and territory formation) are likely more density-dependent than those involving social interactions (e.g. direct pathogen transmission, aggression, and social learning). These findings reveal fundamental ecological rules governing societal structuring, with widespread implications. Identifying scaling rules based on processes that generalise across systems, such as these patterns of density dependence, might provide the ability to predict network structures in novel systems.

ecology↗

bioRxiv2024

Local and global density have distinct and parasite-dependent effects on infection in wild sheep

High density should drive greater parasite exposure. However, evidence linking density with infection generally uses density proxies, rather than of individuals per space within a continuous population. We used a long-term study of wild sheep to link within-population spatiotemporal variation in host density with individual parasite counts. Although four parasites exhibited strong positive relationships with local density, these relationships were mostly restricted to juveniles and faded in adults. Further, one ectoparasite showed strong negative relationships across all age classes. In contrast, population size - a measure of global density - had limited explanatory power, and its effects did not remove those of spatial density, but were complementary. These results indicate that local and global density can exhibit diverse and contrasting effects on infection within populations. Spatial measures of within-population local density may provide substantial additional insight to temporal metrics based on population size, and investigating them more widely could be highly revealing.

ecology↗

bioRxiv2023

Age specific impacts of vegetation functional traits on gastro-intestinal nematode parasite burdens in a large herbivore

O_LIGastro-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 are important in wildlife systems, but the environmental drivers underlying this variation remain poorly understood. C_LIO_LIWe 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 individuals 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. C_LIO_LIEffects 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. C_LIO_LIIn 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. C_LIO_LIOur findings support the importance of fine-scale environmental variation for wildlife disease ecology and provides 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. C_LI

ecology↗

bioRxiv2022

Long-term temporal trends in gastrointestinal parasite infection in wild Soay sheep

Monitoring the prevalence and abundance of parasites over time is important for addressing their potential impact on host life-histories, immunological profiles, and their influence as a selective force. Only long-term ecological studies have the potential to shed light on both the temporal trends in infection prevalence and abundance and the drivers of such trends, because of their ability to dissect drivers that may be confounded over shorter time scales. Despite this, only a relatively small number of such studies exist. Here, we analysed changes in the prevalence and abundance of gastrointestinal parasites in the wild Soay sheep population of St Kilda across 31 years. The host population density has increased across the study, and population density is known to increase parasite transmission, but we found that density and year explained temporal variation in parasite prevalence and abundance independently. Prevalence of both strongyle nematodes and coccidian microparasites increased during the study, and this effect varied between lambs, yearlings and adults. Meanwhile, abundance of strongyles was more strongly linked to host density than to temporal (yearly) dynamics, while abundance of coccidia showed a strong temporal trend without any influence of density. Strikingly, coccidian abundance increased threefold across the course of the study in lambs, while increases in yearlings and adults were negligible. Our decades-long, intensive, individual-based study will enable the role of environmental change and selection pressures in driving these dynamics to be determined, potentially providing unparalleled insight into the drivers of temporal variation in parasite dynamics in the wild. Key findingsO_LIWe studied temporal trends in gastrointestinal parasites of wild sheep over 31 years C_LIO_LIYear and host population density explained temporal variation in parasites independently C_LIO_LIPrevalence of both strongyle nematodes and coccidia varied across the study period C_LIO_LIAbundance of strongyles was more closely linked to host density than year C_LIO_LIAbundance of coccidia increased threefold over time in lambs, but did not vary in adults C_LI

ecology↗

bioRxiv2022

Novel pathogen introduction rapidly alters evolved movement strategies, restructuring animal societies

Animal sociality emerges from individual decisions on how to balance the costs and benefits of being sociable. Movement strategies incorporating social information -- the presence and status of neighbours -- can modulate spatial associations, helping animals avoid infection while benefiting from indirect information about their environment. When a novel pathogen is introduced into a population, it should increase the costs of sociality, selecting against gregariousness. Yet current thinking about novel pathogen introductions into wildlife neglects hosts potential evolutionary responses. We built an individual-based model that captures essential features of the repeated introduction, and subsequent transmission of an infectious pathogen among social hosts. Examining movements in a foraging context, widely shared by many species, we show how introducing a novel pathogen to a population provokes a rapid evolutionary transition to a dynamic social distancing movement strategy. This evolutionary shift triggers a disease-dominated ecological cascade of increased individual movement, decreased resource harvesting, and fewer social encounters. Pathogen-risk adapted individuals form less clustered social networks than their pathogen-risk naive ancestors, which reduces the spread of disease. The mix of post-introduction social movement strategies is influenced by the usefulness of social information and disease cost. Our work demonstrates that evolutionary adaptation to pathogen introductions and re-introductions can be very rapid, comparable to ecological timescales. Our general modelling framework shows why evolutionary dynamics should be considered in movement-disease models, and offers initial predictions for the eco-evolutionary consequences of wildlife pathogen spillover scenarios.

ecology↗

bioRxiv2021

Functionally distinct T-helper cell phenotypes predict resistance to different types of parasites in a wild mammal

O_LIThe adaptive immune system is critical to an effective, long-lasting ability to respond to infection in vertebrates and T-helper (Th) cells play a key role in orchestrating the adaptive immune response. Laboratory studies show that functionally distinct Th responses provide protection against different kinds of parasites (i.e., Th1 responses against microparasites and Th2 against macroparasites). C_LIO_LINatural populations must deal with challenges from a wide range of infectious agents and co-infection with different types of parasite is the norm, so different Th responses are likely to play an important and dynamic role in maintaining host health and fitness. However, the relationship between T helper immune phenotypes and infection with different types of parasites remains poorly understood in wild animals. C_LIO_LIIn this study, we characterised variation in functionally distinct Th responses (Th1, Th2, Th17 and regulatory responses) in a wild population of Soay sheep using flow cytometry to detect Th-subset specific transcription factors, and ex vivo lymphocyte stimulation to quantify release of Th-associated cytokines. We specifically tested the prediction that raised Th1 and Th2 responses should predict reduced apicomplexan (coccidian) and helminth (nematode) parasite burdens, respectively. C_LIO_LICell counts of different Th subsets measured by flow cytometry did not vary with age or sex. However, all measures of Th-associated ex vivo cytokine production increased with age, and Th17- and regulatory Th-associated cytokine production increased more rapidly with age in males than females. C_LIO_LIIndependent of age and sex, Th2-associated immune measures negatively predicted gastro-intestinal strongyle nematode faecal egg count, while production of the Th1-associated cytokine IFN-{gamma} negatively predicted coccidian faecal oocyst count. C_LIO_LIOur results provide important support from outside the laboratory that Th1 and Th2 responses confer resistance to different kinds of parasites (micro- and macro-parasites, respectively). They also add to mounting evidence from wild populations that Th1/Th2 trade-offs often observed in controlled laboratory experiments may not readily translate to more complex natural systems. C_LIO_LIOur study illustrates that harnessing more specific reagents and tools from laboratory immunology has the potential to illuminate our understanding of epidemiology and host-parasite co-evolution in the wild. C_LI

ecology↗

bioRxiv2021

Seasonal dynamics and repeatability of gastrointestinal parasite burdens in wild Soay sheep

Seasonality is a ubiquitous feature of wildlife disease ecology, but is determined by a complex interplay of environmental, parasitological and host factors. Gastrointestinal parasites often exhibit strong seasonal dynamics in wild vertebrate populations due to, for example, environmental influences on free-living or vectored life stages, and variation in the physiological and immune status of hosts across their annual cycle. At the same time, wild populations are typically infected with multiple parasites. The seasonal dynamics of co-infecting parasites may differ depending on age and reproductive status, and associations among parasites may be driven by short-term within-individual changes or longer-term interactions that are consistent among hosts. Here, we used faecal samples and egg counts collected repeatedly from individually marked and monitored wild Soay sheep that were part of a long-term study to investigate seasonal dynamics of six gastrointestinal parasite groups (strongyle nematodes, coccidian protozoa, Capillaria, Strongyloides, Nematodirus, and Moniezia). Prevalence and abundance generally tended to be higher spring and summer, and burdens were higher in lambs than adults. Within the highly prevalent strongyle nematode group, we found differences in seasonality of egg counts depending on adult reproductive status. Reproductive ewes had increased counts in spring around the time of birth followed by a drop in abundance in summer, while barren ewes showed little evidence of seasonality. Males showed a sustained rise in egg counts through spring and summer, and sex differences were only strongly apparent in summer. In contrast, in similarly prevalent coccidia we found a peak in faecal oocyst counts in spring but no differences in seasonality among males, barren and pregnant ewes. Using multivariate mixed-effects models, we went on to show that both strongyle and coccidia counts are moderately repeatable across seasons among individuals. We further show that apparent positive correlation between strongyle and coccidia counts was driven by short-term within-individual changes in both parasite burdens rather than long-term among-individual covariation. Overall, our results demonstrate that seasonality varies across demographic and parasite groups and highlight the value of investigating fluctuating susceptibility and exposure over time for understanding epidemiology of a population.

ecology↗

bioRxiv2021

Data proliferation, reconciliation, and synthesis in viral ecology

The fields of viral ecology and evolution have rapidly expanded in the last two decades, driven by technological improvements, and motivated by efforts to discover potentially zoonotic wildlife viruses under the rubric of pandemic prevention. One consequence has been a massive proliferation of host-virus association data, which comprise the backbone of research in viral macroecology and zoonotic risk prediction. These data remain fragmented across numerous data portals and projects, each with their own scope, structure, and reporting standards. Here, we propose that synthesis of host-virus association data is a central challenge to improve our understanding of the global virome and develop foundational theory in viral ecology. To illustrate this, we build an open reconciled mammal-virus database from four key published datasets, applying a standardized taxonomy and metadata. We show that reconciling these datasets provides a substantially richer view of the mammal virome than that offered by any one individual database. We argue for a shift in best practice towards the incremental development and use of synthetic datasets in viral ecology research, both to improve comparability and replicability across studies, and to facilitate future efforts to use machine learning to predict the structure and dynamics of the global virome.

ecology↗

bioRxiv2021

Urban-adapted mammal species have more known pathogens

The world is rapidly urbanising, inviting mounting concern that urban environments will experience increased zoonotic disease risk. Urban animals could have more frequent contact with humans, and therefore may transmit more zoonotic parasites; however, these animals have a specific set of underlying traits that may determine their parasite burdens while predisposing them to urban living, and they may be subject to more intense research effort, both of which could complicate our ability to reliably identify the role of urbanisation in driving zoonotic risk. Here, we test whether urban mammal species host more known zoonotic parasites, investigating the potential underlying drivers while accounting for a correlated suite of phenotypic, taxonomic, and geographic predictors. We found that urban-adapted mammals have more documented parasites, and more zoonotic parasites specifically: despite comprising only 157 of the 2792 investigated species (6%), urban mammals provided 39% of known host-parasite combinations and showed consistently higher viral discovery rates throughout the last century. However, contrary to predictions, much of the observed effect was attributable to research effort rather than to urban adaptation status itself, and urban-adapted species in fact hosted fewer zoonoses than expected given their total observed parasite richness. We conclude that extended historical contact with humans has had a limited impact on the number of observed zoonotic parasites in urban-adapted mammals; instead, their greater observed zoonotic richness likely reflects sampling bias arising from proximity to humans, which supports a near-universal underlying pattern of conflation between zoonotic risk, research effort, and synanthropy. These findings underscore the need to resolve the ecological mechanisms underlying links between anthropogenic change, sampling bias, and observed wildlife disease dynamics.

ecology↗

bioRxiv2020

A mixed model approach for estimating drivers of microbiota community composition and differential taxonomic abundance

O_LINext-generation sequencing (NGS) and meta-barcoding approaches have revolutionized understanding of within-host communities, such as the gut microbiome, in humans and laboratory animals. The application of such approaches in wild animal populations is growing, but there is a disconnect between the widely-applied generalised linear mixed model (GLMM) approaches commonly used to study phenotypic variation and the statistical toolkit from community ecology which is typically applied to meta-barcoding data. C_LIO_LIHere, we describe and illustrate a novel GLMM-based approach for analysing the taxon-specific sequence read counts derived from standard meta-barcoding data. This approach allows us to decompose the contribution of different drivers of variation in community structure (e.g. year, season, individual host), via interaction terms in the random effects structure of the model. We also show how these models can be used to determine the degree to which specific taxa or taxonomic groups are responsible for variance attributed to different drivers. C_LIO_LITo illustrate this approach, we applied it to two cross-sectional meta-barcoding data sets from the Soay Sheep population of St. Kilda. The GLMM approach yielded results that were in agreement with more classical approaches from community ecology, showing that variation the gut microbiota community in these sheep was better explained by age group than by season. We were able to quantify the contributions of different sources of variation to community structure, and also to drill down into the model predictions to show that the age effects we observed were principally due to increases in taxa of the phyla Bacteroidetes and declines in taxa of the phyla Firmicutes. C_LIO_LIOur proposed models offer a powerful new approach to understanding the drivers of variation in estimates of community structure derived from meta-barcoding data. We discuss how our approach could be readily adapted to allow researchers to estimate that contribution of host genotype, environment, and microbial/parasite phylogeny to observed community structure, and thus provide a powerful means to answer emerging questions surrounding the ecological and evolutionary roles of within-host communities. C_LI

evolutionary biology↗

bioRxiv2020

Experimental parasite community perturbation reveals associations between Sin Nombre virus and gastrointestinal nematodes in a rodent reservoir host

Individuals are often co-infected with several parasite species, yet measuring within-host interactions remains difficult in the wild. Consequently, such interactions impacts on host fitness and epidemiology are often unknown. We used anthelmintic drugs to experimentally reduce nematode infection and measured the effects on both nematodes and the important zoonosis Sin Nombre virus (SNV) in its primary wild reservoir (Peromyscus spp.). Treatment significantly reduced nematode infection, but increased SNV seroprevalence. Furthermore, mice that were co-infected with both nematodes and SNV were in better condition and survived as much as four times longer than mice infected with either parasite alone. These results highlight the importance of investigating multiple parasites for understanding interindividual variation and epidemiological dynamics in reservoir populations with zoonotic transmission potential.

ecology↗

bioRxiv2020

Spatiotemporal variation in drivers of parasitism in a wild wood mouse population

O_LIHost-parasite interactions in nature are driven by a range of factors across several ecological scales, so observed relationships are often context-dependent. Importantly, if these factors vary across space and time, practical sampling limitations can limit or bias inferences, and the relative importance of different drivers can be hard to discern. C_LIO_LIWe collected a replicated, longitudinal dataset of >1000 individual wood mice (Apodemus sylvaticus) encompassing 6 years of sampling across 5 different woodland sites to investigate how environmental, host and within-host factors determine infection intensity of a highly prevalent gastrointestinal nematode, Heligmosomoides polygyrus. C_LIO_LIWe used a Bayesian modelling approach to further quantify if and how each factor varied in space and time. Finally, we examined the extent to which a lack of spatially or temporally replication (i.e., within single years or single sites) and single (cross-sectional) versus repeated (longitudinal) sampling of individuals would affect which drivers were found to predict H. polygyrus infection. C_LIO_LISeason, host body condition, and sex were the three most important determinants of infection intensity; however, the strength and even direction of these effects varied in time, but not in space. Additionally, longitudinal datasets, in which we can control for within-individual variation through repeat observations, provided more robust estimates of the drivers of parasite intensity compared to cross-sectional data. C_LIO_LIThese results highlight the importance of accounting for spatiotemporal variation in drivers of disease dynamics and the need to incorporate spatiotemporal replication when designing sampling regimes. Furthermore, they suggest that embracing rather than simply controlling for spatiotemporal variation can reveal important insight into host-parasite relationships in the wild. C_LI

ecology↗

bioRxiv2019

Supplemented nutrition increases immunity and drug efficacy in a natural host-helminth system

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 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 resistance to the gastrointestinal nematode Heligmosomoides polygyrus and anthelmintic treatment efficacy in both natural and captive populations. Supplemented wood mice were more resistant to H. polygyrus infection, cleared worms more efficiently after treatment, produced stronger general and parasite-specific antibody responses, and maintained better body condition. In addition, supplemented nutrition in conjunction with anthelminthic treatment significantly reduced H. polygyrus transmission potential. These large-scale improvements in condition and immunity of supplemented nutrition found in controlled and wild environments show the rapid and extensive benefits of a well-balanced diet and have important implications for using diet interventions to improve disease control programmes. Author SummaryGastrointestinal helminths are ubiquitous parasites which cause chronic infections and debilitating symptoms worldwide for human and animal populations alike. Efforts to control helminth infections rely primarily on deworming drugs. However, despite high availability and low cost of these drugs, reinfection is common and helminths remain a substantial problem in many areas of the world. One factor which contributes to the persistence of helminth infections is co-occurrence of malnutrition. Extensive work in model laboratory systems has shown that deficiencies in both macro- and micronutrients can impair host immune responses to helminth infections, but how this relationship translates to natural host-helminth systems and drug efficacy is still poorly understood. Here, we used a combination of experimental nutrition supplementation and deworming treatment in paired wood mouse populations in both wild and captive environments to determine the role of a well-balanced diet for infection control in a natural host-helminth system. We found that mice on a supplemented diet had lower burden of infection and increased drug efficacy, body condition, and immune responses. We also found that supplementation lowered transmission potential of hosts. These broad and rapid effects of increased nutrition quality have important implications for the benefits of diet interventions alongside deworming drugs.

ecology↗