skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: Immune interactions and heterogeneity in transmission drives the pathogen‐mediated invasion of grey squirrels in the UK
Abstract Mathematical models highlighted the importance of pathogen‐mediated invasion, with the replacement of red squirrels by squirrelpox virus (SQPV) carrying grey squirrels in the UK, a well‐known example.In this study, we combine new epidemiological models, with a range of infection characteristics, with recent longitudinal field and experimental studies on the SQPV dynamics in red and grey squirrel populations to better infer the mechanistic basis of the disease interaction.A key finding is that a model with either partial immunity or waning immunity and reinfection, where individuals become seropositive on the second exposure to infection, that up to now has been shown in experimental data only, can capture the key aspects of the field study observations.By fitting to SQPV epidemic observations in isolated red squirrel populations, we can infer that SQPV transmission between red squirrels is significantly (4×) higher than the transmission between grey squirrels and as a result our model shows that disease‐mediated replacement of red squirrels by greys is considerably more rapid than replacement in the absence of SQPV.Our findings recover the key results of the previous model studies, which highlights the value of simple strategic models that are appropriate when there are limited data, but also emphasise the likely complexity of immune interactions in wildlife disease and how models can help infer disease processes from field data.  more » « less
Award ID(s):
2011109
PAR ID:
10524022
Author(s) / Creator(s):
; ; ;
Publisher / Repository:
Wiley
Date Published:
Journal Name:
Journal of Animal Ecology
Volume:
93
Issue:
6
ISSN:
0021-8790
Page Range / eLocation ID:
663 to 675
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract Determining parameters that govern pathogen transmission (such as the force of infection, FOI), and pathogen impacts on morbidity and mortality, is exceptionally challenging for wildlife. Vital parameters can vary, for example across host populations, between sexes and within an individual's lifetime.Feline immunodeficiency virus (FIV) is a lentivirus affecting domestic and wild cat species, forming species‐specific viral–host associations. FIV infection is common in populations of puma (Puma concolor), yet uncertainty remains over transmission parameters and the significance of FIV infection for puma mortality. In this study, the age‐specific FOI of FIV in pumas was estimated from prevalence data, and the evidence for disease‐associated mortality was assessed.We fitted candidate models to FIV prevalence data and adopted a maximum likelihood method to estimate parameter values in each model. The models with the best fit were determined to infer the most likely FOI curves. We applied this strategy for female and male pumas from California, Colorado, and Florida.When splitting the data by sex and area, our FOI modeling revealed no evidence of disease‐associated mortality in any population. Both sex and location were found to influence the FOI, which was generally higher for male pumas than for females. For female pumas at all sites, and male pumas from California and Colorado, the FOI did not vary with puma age, implying FIV transmission can happen throughout life; this result supports the idea that transmission can occur from mothers to cubs and also throughout adult life. For Florida males, the FOI was a decreasing function of puma age, indicating an increased risk of infection in the early years, and a decreased risk at older ages.This research provides critical insight into pathogen transmission and impact in a secretive and solitary carnivore. Our findings shed light on the debate on whether FIV causes mortality in wild felids like puma, and our approach may be adopted for other diseases and species. The methodology we present can be used for identifying likely transmission routes of a pathogen and also estimating any disease‐associated mortality, both of which can be difficult to establish for wildlife diseases in particular. 
    more » « less
  2. Abstract The prevalence and intensity of parasites in wild hosts varies across space and is a key determinant of infection risk in humans, domestic animals and threatened wildlife. Because the immune system serves as the primary barrier to infection, replication and transmission following exposure, we here consider the environmental drivers of immunity. Spatial variation in parasite pressure, abiotic and biotic conditions, and anthropogenic factors can all shape immunity across spatial scales. Identifying the most important spatial drivers of immunity could help pre‐empt infectious disease risks, especially in the context of how large‐scale factors such as urbanization affect defence by changing environmental conditions.We provide a synthesis of how to apply macroecological approaches to the study of ecoimmunology (i.e. macroimmunology). We first review spatial factors that could generate spatial variation in defence, highlighting the need for large‐scale studies that can differentiate competing environmental predictors of immunity and detailing contexts where this approach might be favoured over small‐scale experimental studies. We next conduct a systematic review of the literature to assess the frequency of spatial studies and to classify them according to taxa, immune measures, spatial replication and extent, and statistical methods.We review 210 ecoimmunology studies sampling multiple host populations. We show that whereas spatial approaches are relatively common, spatial replication is generally low and unlikely to provide sufficient environmental variation or power to differentiate competing spatial hypotheses. We also highlight statistical biases in macroimmunology, in that few studies characterize and account for spatial dependence statistically, potentially affecting inferences for the relationships between environmental conditions and immune defence.We use these findings to describe tools from geostatistics and spatial modelling that can improve inference about the associations between environmental and immunological variation. In particular, we emphasize exploratory tools that can guide spatial sampling and highlight the need for greater use of mixed‐effects models that account for spatial variability while also allowing researchers to account for both individual‐ and habitat‐level covariates.We finally discuss future research priorities for macroimmunology, including focusing on latitudinal gradients, range expansions and urbanization as being especially amenable to large‐scale spatial approaches. Methodologically, we highlight critical opportunities posed by assessing spatial variation in host tolerance, using metagenomics to quantify spatial variation in parasite pressure, coupling large‐scale field studies with small‐scale field experiments and longitudinal approaches, and applying statistical tools from macroecology and meta‐analysis to identify generalizable spatial patterns. Such work will facilitate scaling ecoimmunology from individual‐ to habitat‐level insights about the drivers of immune defence and help predict where environmental change may most alter infectious disease risk. 
    more » « less
  3. Abstract The spatial organization of populations determines their pathogen dynamics. This is particularly important for communally roosting species, whose aggregations are often driven by the spatial structure of their environment.We develop a spatially explicit model for virus transmission within roosts of Australian tree‐dwelling bats (Pteropusspp.), parameterized to reflect Hendra virus. The spatial structure of roosts mirrors three study sites, and viral transmission between groups of bats in trees was modelled as a function of distance between roost trees. Using three levels of tree density to reflect anthropogenic changes in bat habitats, we investigate the potential effects of recent ecological shifts in Australia on the dynamics of zoonotic viruses in reservoir hosts.We show that simulated infection dynamics in spatially structured roosts differ from that of mean‐field models for equivalently sized populations, highlighting the importance of spatial structure in disease models of gregarious taxa. Under contrasting scenarios of flying‐fox roosting structures, sparse stand structures (with fewer trees but more bats per tree) generate higher probabilities of successful outbreaks, larger and faster epidemics, and shorter virus extinction times, compared to intermediate and dense stand structures with more trees but fewer bats per tree. These observations are consistent with the greater force of infection generated by structured populations with less numerous but larger infected groups, and may flag an increased risk of pathogen spillover from these increasingly abundant roost types.Outputs from our models contribute insights into the spread of viruses in structured animal populations, like communally roosting species, as well as specific insights into Hendra virus infection dynamics and spillover risk in a situation of changing host ecology. These insights will be relevant for modelling other zoonotic viruses in wildlife reservoir hosts in response to habitat modification and changing populations, including coronaviruses like SARS‐CoV‐2. 
    more » « less
  4. Abstract Controlling persistent infectious disease in wildlife populations is an ongoing challenge for wildlife managers and conservationists worldwide, and chronic diseases in particular remain a pernicious problem.Here, we develop a dynamic pathogen transmission model capturing key features ofMycoplasma ovipneumoniaeinfection, a major cause of population declines in North American bighorn sheepOvis canadensis. We explore the effects of model assumptions and parameter values on disease dynamics, including density‐ versus frequency‐dependent transmission, the inclusion of a carrier class versus a longer infectious period, host survival rates, disease‐induced mortality and recovery rates and the epidemic growth rate. Along the way, we estimate the basic reproductive ratio,R0, forM. ovipneumoniaein bighorn sheep to fall between approximately 1.36 and 1.74.We apply the model to compare efficacies across a suite of management actions following an epidemic, including test‐and‐remove, depopulation‐and‐reintroduction, range expansion, herd augmentation and density reduction.Our results suggest that test‐and‐remove, depopulation‐and‐reintroduction and range expansion could help persistently infected bighorn sheep herds recovery following an epidemic. By contrast, augmentation could lead to worse outcomes than those expected in the absence of management. Other management actions that improve host survival or reduce disease‐induced mortality are also likely to improve population size and persistence of chronically infected herds.Synthesis and applications. Dynamic transmission models like the one employed here offer a structured, logical approach for exploring hypotheses, planning field experiments and designing adaptive management. We find that management strategies that removed infected animals or isolated them within a structured metapopulation were most successful at facilitating herd recovery from a low‐prevalence, chronic pathogen. Ideally, models like ours should operate iteratively with field experiments to triangulate on better approaches for managing wildlife diseases. 
    more » « less
  5. Abstract Long‐term studies of wild animals provide the opportunity to investigate how phenotypic plasticity is used to cope with environmental fluctuations and how the relationships between phenotypes and fitness can be dependent upon the ecological context.Many previous studies have only investigated life‐history plasticity in response to changes in temperature, yet wild animals often experience multiple environmental fluctuations simultaneously. This requires field experiments to decouple which ecological factor induces plasticity in fitness‐relevant traits to better understand their population‐level responses to those environmental fluctuations.For the past 32 years, we have conducted a long‐term integrative study of individually marked North American red squirrelsTamiasciurus hudsonicusErxleben in the Yukon, Canada. We have used multi‐year field experiments to examine the physiological and life‐history responses of individual red squirrels to fluctuations in food abundance and conspecific density.Our long‐term observational study and field experiments show that squirrels can anticipate increases in food availability and density, thereby decoupling the usual pattern where animals respond to, rather than anticipate, an ecological change.As in many other study systems, ecological factors that can induce plasticity (such as food and density) covary. However, our field experiments that manipulate food availability and social cues of density (frequency of territorial vocalizations) indicate that increases in social (acoustic) cues of density in the absence of additional food can induce similar life‐history plasticity, as does experimental food supplementation.Changes in the levels of metabolic hormones (glucocorticoids) in response to variation in food and density are one mechanism that seems to induce this adaptive life‐history plasticity.Although we have not yet investigated the energetic response of squirrels to elevated density or its association with life‐history plasticity, energetics research in red squirrels has overturned several standard pillars of knowledge in physiological ecology.We show how a tractable model species combined with integrative studies can reveal how animals cope with resource fluctuations through life‐history plasticity. 
    more » « less