How to Live with the Enemy: Understanding Tolerance to Parasites

Råberg, Lars

doi:10.1371/journal.pbio.1001989

Cited by 141 publications

(161 citation statements)

References 24 publications

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“…However, our study focused on short‐term resistance to trematode infection. While individuals from populations further from agriculture with higher inducible tolerance and lower baseline tolerance were less resistant to trematodes, they could display higher levels of parasite clearance or tolerance compared to individuals from populations closer to agriculture with lower inducible tolerance and higher baseline tolerance (Raberg, 2014). Integrating short‐term (i.e., resistance) and long‐term parameters (i.e., clearance and tolerance) will provide a more complete understanding of how evolved pesticide tolerance influences host–trematode interactions.…”

Section: Discussionmentioning

confidence: 99%

Evolved pesticide tolerance influences susceptibility to parasites in amphibians

Hua

Wuerthner

Jones

et al. 2017

Evolutionary Applications

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Because ecosystems throughout the globe are contaminated with pesticides, there is a need to understand how natural populations cope with pesticides and the implications for ecological interactions. From an evolutionary perspective, there is evidence that pesticide tolerance can be achieved via two mechanisms: selection for constitutive tolerance over multiple generations or by inducing tolerance within a single generation via phenotypic plasticity. While both mechanisms can allow organisms to persist in contaminated environments, they might result in different performance trade‐offs including population susceptibility to parasites. We have identified 15 wood frog populations that exist along a gradient from close to agriculture and high, constitutive pesticide tolerance to far from agriculture and inducible pesticide tolerance. Using these populations, we investigated the relationship between evolutionary responses to the common insecticide carbaryl and host susceptibility to the trematode Echinoparyphium lineage 3 and ranavirus using laboratory exposure assays. For Echinoparyphium, we discovered that wood frog populations living closer to agriculture with high, constitutive tolerance experienced lower loads than populations living far from agriculture with inducible pesticide tolerance. For ranavirus, we found no relationship between the mechanism of evolved pesticide tolerance and survival, but populations living closer to agriculture with high, constitutive tolerance experienced higher viral loads than populations far from agriculture with inducible tolerance. Land use and mechanisms of evolved pesticide tolerance were associated with susceptibility to parasites, but the direction of the relationship is dependent on the type of parasite, underscoring the complexity between land use and disease outcomes. Collectively, our results demonstrate that evolved pesticide tolerance can indirectly influence host–parasite interactions and underscores the importance of including evolutionary processes in ecotoxicological studies.

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Section: Discussionmentioning

confidence: 99%

Evolved pesticide tolerance influences susceptibility to parasites in amphibians

Hua

Wuerthner

Jones

et al. 2017

Evolutionary Applications

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“…The persistence of a non-symptomatic density of ENV in the A. plantaginis gut may raise questions about the relationship between a host's pathogen tolerance and it's pathogen resistance (Schneider & Ayres 2008, Vale et al 2014, Råberg 2014. A host's ability to withstand a certain pathogen density level (tolerance) could be a more adaptive solution compared to a complete clearance (resistance), if the clearance-associated costs outweigh the benefits (Vale et al 2014).…”

Section: Discussionmentioning

confidence: 99%

“…While these approaches have yielded tremendous benefits, alone it may bias our understanding of innate immunity. It may be that different strategies of pathogen resistance and tolerance have evolved (Råberg 2014), and that these differences have been overlooked. Lepidopterans, like other insects, activate their immune defence against microorganisms by recognizing the pathogen surface structure with an array of binding proteins.…”

Section: Introductionmentioning

confidence: 99%

Lepidopteran species have a variety of defence strategies against bacterial infections

Mikonranta

Dickel

Mappes

et al. 2017

Journal of Invertebrate Pathology

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“…Organisms can defend themselves from a pathogen via two mechanisms, which are not mutually exclusive: resistance and tolerance (Schneider & Ayres 2008;Råberg 2014). While resistance mechanisms prevent infection or limit pathogen growth, tolerance mechanisms limit fitness effects of a given pathogen burden.…”

Section: Discussionmentioning

confidence: 99%

“…Tolerance is an alternative strategy for hosts to respond to a pathogen, in which the fitness effects of infection are reduced or controlled despite high pathogen burdens (Medzhitov et al 2012, Råberg 2014). …”

Section: Variation In Susceptibility To Chytridiomycosismentioning

confidence: 99%

Interactions between amphibian skin sloughing and a cutaneous fungal disease: infection progression, immune defence, and phylogenetic patterns

Ohmer¹

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Worldwide, there has been an unprecedented rise in emerging infectious diseases of wildlife, and this has contributed to a widespread biodiversity crisis. Amphibian populations, in particular, are threatened by the fungal pathogen Batrachochytrium dendrobatidis (Bd), which in post-metamorphic animals only infects the skin, and causes the potentially lethal disease chytridiomycosis. Amphibians regularly slough their skin, and in doing so remove many skinassociated microbes. Thus, skin sloughing may play an important role in the pathogenesis of chytridiomycosis. To investigate this association, the influence of Bd infection on amphibian skin sloughing, and the role of sloughing in regulating infection, was examined. Furthermore, to better understand the variation in skin sloughing rates across species and ecological groups, and make inferences about the role of this process in susceptibility to this fungal disease, amphibian skin structure and function was investigated within a phylogenetic context. To determine the relationship between skin sloughing and disease progression (chapter 2), adult green tree frogs (Litoria caerulea) were exposed to an Australian Bd strain, and sloughing rates and infection load were monitored on a naturalistic cycling temperature regime (15 -23˚C).Sloughing rates were determined by filming frogs and infection intensity was monitored before and after sloughing with conventional swabbing and quantitative PCR. Sloughing rate was found to increase with Bd infection load in infected frogs, but sloughing itself did not affect Bd load on the ventral skin surface. Although a faster sloughing rate might be considered advantageous for Bdinfected animals, it does not appear to curb the progression of disease in susceptible species. In fact, sloughing may actually contribute to the loss of physiological homeostasis seen in terminally ill frogs by further inhibiting water and electrolyte transport across the skin.In some species less susceptible to chytridiomycosis, it has been demonstrated that Bd growth remains epibiotic, without penetrating the underlying epidermal layers. Therefore, sloughing may more effectively remove Bd zoospores in less susceptible species (chapter 3). To test this hypothesis, five Australian frog species, Lit. caerulea, Platyplectrum ornatum, Lechriodus fletcheri, Limnodynastes peronii, and Lim. tasmaniensis, were exposed to an Australian Bd strain, and their sloughing rates and infection loads monitored over time. Utilising an improved methodology to remove any artefacts from the swabbing itself, sloughing was found to reduce Bd load on the ventral skin surface, in all five species, despite wide ranging variation in susceptibility to Bd infection and subsequent disease. In less susceptible species, sloughing reduced Bd load up to 100%, leading to infection clearance. However, the drop in Bd load was only temporary in susceptible species, potentially due to the invasive growth of Bd in skin layers underlying the ii stratum corneum in these species. If less suscept...

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How to Live with the Enemy: Understanding Tolerance to Parasites

Abstract: This Primer examines the phenomenon of infection tolerance and discusses three recent PLOS Biology research articles about the causes and consequences of variation in tolerance in natural populations.

Cited by 141 publications

References 24 publications

Evolved pesticide tolerance influences susceptibility to parasites in amphibians

Evolved pesticide tolerance influences susceptibility to parasites in amphibians

Lepidopteran species have a variety of defence strategies against bacterial infections

Interactions between amphibian skin sloughing and a cutaneous fungal disease: infection progression, immune defence, and phylogenetic patterns

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