Infections on the move: how transient phases of host movement influence disease spread

Daversa, David R.; Fenton, Andy; Dell, A. I.; Garner, Trenton W. J.; Manica, Andrea

doi:10.1098/rspb.2017.1807

Cited by 52 publications

(61 citation statements)

References 69 publications

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“…These small-scale spatiotemporal variations may alter the local disease ecology (i.e. prevalence and intensity of infection) by facilitating or compressing opportunities for pathogen transmission and/or growth (Daversa, Fenton, Dell, Garner, & Manica, 2017;Daversa, Manica, Bosch, Jolles, & Garner, 2018). Beyond climatic patterns, anthropogenic habitat disturbance may cause a cascade of factors that exacerbate infectious disease emergence.…”

Section: Introductionmentioning

confidence: 99%

Spatiotemporal heterogeneity decouples infection parameters of amphibian chytridiomycosis

McMillan

Lesbarrères

Harrison

et al. 2020

Journal of Animal Ecology

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Emerging infectious diseases are responsible for declines in wildlife populations around the globe. Mass mortality events associated with emerging infectious diseases are often associated with high number of infected individuals (prevalence) and high pathogen loads within individuals (intensity). At the landscape scale, spatial and temporal variation in environmental conditions can alter the relationship between these infection parameters and blur the overall picture of disease dynamics. Quantitative estimates of how infection parameters covary with environmental heterogeneity at the landscape scale are scarce. If we are to identify wild populations at risk of disease epidemics, we must elucidate the factors that shape, and potentially decouple, the link between pathogen prevalence and intensity of infection over complex ecological landscapes. Using a network of 41 populations of the amphibian host Rana pipiens in Ontario, Canada, we present the spatial and temporal heterogeneity in pathogen prevalence and intensity of infection of the chytrid fungus Batrachochytrium dendrobatidis (Bd), across a 3‐year period. We then quantify how covariation between both infection parameters measured during late summer is modified by previously experienced spatiotemporal environmental heterogeneity across 14 repeat sampled populations. Late summer Bd infection parameters are governed, at least in part, by different environmental factors operating during separate host life‐history events. Our results provide evidence for a relationship between Bd prevalence and thermal regimes prior to host breeding at the site level, and a relationship between intensity of infection and aquatic conditions (precipitation, hydroshed size and river density) throughout host breeding period at the site level. This demonstrates that microclimatic variation within temporal windows can drive divergent patterns of pathogen dynamics within and across years, by effecting changes in host behaviour which interfere with the pathogen's ability to infect and re‐infect hosts. A clearer understanding of the role that spatiotemporal heterogeneity has upon infection parameters will provide valuable insights into host–pathogen epidemiology, as well as more fundamental aspects of the ecology and evolution of interspecific interactions.

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Section: Introductionmentioning

confidence: 99%

Spatiotemporal heterogeneity decouples infection parameters of amphibian chytridiomycosis

McMillan

Lesbarrères

Harrison

et al. 2020

Journal of Animal Ecology

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“…or through new environments that facilitate recovery from infection [19,20]. Conversely, individuals may also encounter novel parasites as they migrate to or through new habitats [21 -23].…”

Section: Introductionmentioning

confidence: 99%

Metrics matter: the effect of parasite richness, intensity and prevalence on the evolution of host migration

et al. 2018

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Parasites have long been thought to influence the evolution of migration, but precisely determining the conditions under which this occurs by quantifying costs of infection remains a challenge. Here we developed a model that demonstrates how the metric used to describe infection (richness/diversity, prevalence or intensity) shapes the prediction of whether migration will evolve. The model shows that predictions based on minimizing richness yield opposite results compared to those based on minimizing prevalence, with migration only selected for when minimizing prevalence. Consistent with these findings, empirical studies that measure parasite diversity typically find that migrants are worse off than residents, while those measuring prevalence or intensity find the opposite. Our own empirical analysis of fish parasite data finds that migrants (of all types) have higher parasite richness than residents, but with no significant difference in either prevalence or intensity. BackgroundMigration is a ubiquitous behaviour that spans a large range of temporal and spatial scales [1]. Although stereotypical images of migration often feature birds moving to the equator for the winter and ungulates travelling across African savannahs, migratory behaviour is a much broader phenomenon. Amphibians have small-scale migrations between aquatic and terrestrial habitats [2], as do many land crabs [3]; moths migrate altitudinally to escape seasonally hot conditions [4]; plankton migrate daily up and down in the water column [5]; and some sea lions migrate to breed every 17-18 months [6]. The uniqueness of migration comes from the predictable and directional nature of the movement. However, movement of all forms can be inherently costly in terms of depleting energy, reducing survival and increasing exposure to novel and uncertain conditions [7].Why, then, do organisms migrate? Three broad sets of factors are thought to shape migration [8]. First, some species migrate between breeding/spawning grounds and areas that are better suited to adult survival or resource accumulation. Second, some species are constantly on the move tracking changing resource patterns. Third, some species spend part of the year in one area that is well suited for breeding and foraging, but migrate away to seek refuge (from cold, dry or stormy weather) during part of the year. Both early and modern conceptions of migration as a refuge behaviour focus on climate as a driving factor [8,9]. However, these seasonal movements may also be driven by predators [10,11], parasitoids [12], or parasites and pathogens [13].The role of parasites in determining host ecology and behaviour is becoming increasingly recognized [14,15]. Parasites (which here we define broadly to include both macroparasites and microparasites, as per [16]) in particular can shape migration patterns in several distinct ways. By migrating, individuals can escape parasites that are restricted to certain habitats [17,18], or move to

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“…Understanding how pathogens spread through populations remains a fundamental challenge. The extent to which pathogen spread reflects movement patterns of their hosts is enigmatic but important for controlling disease 1, 2 . If pathogen spread mirrors host gene flow, host genetic structure/differentiation could be a valuable proxy for pathogen spread and be used as a basis to inform disease control 3, 4 (e.g., male vampire bat [ Desmodus rotundus ] genetics closely mirrors phylogenetic structure of rabies 5 ).…”

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Host relatedness and landscape connectivity shape pathogen spread in a large secretive carnivore

Fountain-Jones

Kraberger

Gagne

et al. 2019

Preprint

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Urban expansion can fundamentally alter wildlife movement and gene flow, but how urbanization alters pathogen spread is poorly understood. Here we combine high resolution host and viral genomic data with landscape variables to examine the context of viral spread in puma from two contrasting regions: one bounded by the wildland urban interface (WUI) and one unbounded with minimal anthropogenic development. We found landscape variables and host gene flow explained significant amounts of variation of feline immunodeficiency virus (FIV) spread in the WUI, but not in the unbounded region. The most important predictors of viral spread also differed; host spatial proximity, host relatedness, and mountain ranges played a role in FIV spread in the WUI, whereas unpaved roads were more important in the unbounded region. Our research demonstrates how anthropogenic landscapes can alter pathogen spread, providing a more nuanced understanding of host-pathogen relationships to inform disease ecology in free-ranging species.

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Infections on the move: how transient phases of host movement influence disease spread

Cited by 52 publications

References 69 publications

Spatiotemporal heterogeneity decouples infection parameters of amphibian chytridiomycosis

Spatiotemporal heterogeneity decouples infection parameters of amphibian chytridiomycosis

Metrics matter: the effect of parasite richness, intensity and prevalence on the evolution of host migration

Host relatedness and landscape connectivity shape pathogen spread in a large secretive carnivore

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