Reduced immune function predicts disease susceptibility in frogs infected with a deadly fungal pathogen

Savage, Anna E.; Terrell, Kimberly A.; Gratwicke, Brian; Mattheus, Nichole M.; Augustine, Lauren; Fleischer, Robert C.

doi:10.1093/conphys/cow011

Cited by 33 publications

(40 citation statements)

References 70 publications

(97 reference statements)

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“…On one hand, natural variation in temperature impacts the expression of amphibian immunity and influences susceptibility to disease (Maniero and Carey, 1997;Raffel et al, 2006). On the other hand, warmer temperatures decrease the activity period and lifespan of Bd zoospores (Woodhams et al, 2008; Rollins-Smith et al, 2015), but they may rely on adaptive immunity, as has been shown for other frogs (Savage and Zamudio, 2011;Ellison et al, 2014;McMahon et al, 2014;Savage et al, 2016). The fact that we found a positive relationship between previous exposure and Bd infection intensity during the experiment indicates that acquired immunity may not confer full resistance to coqui frogs (Figure 4), because individuals still get infected when challenged with the pathogen at high doses.…”

Section: Discussionmentioning

confidence: 94%

Environmental fluctuations and host skin bacteria shift survival advantage between frogs and their fungal pathogen

2016

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Fluctuating environments can modulate host-pathogen interactions by providing a temporary advantage to one of the interacting organisms. However, we know very little about how environmental conditions facilitate beneficial interactions between hosts and their microbial communities, resulting in individual persistence with a particular pathogen. Here, we experimentally infected Eleutherodactylus coqui frogs with the fungal pathogen Batrachochytrium dendrobatidis (Bd) under environmental conditions known to confer the survival advantage to the host during the warm-wet season, or alternatively to the pathogen during the cool-dry season. We used 16S rRNA amplicon sequencing to quantify changes in bacterial richness and phylogenetic diversity, and identified operational taxonomic units (OTUs) that became overrepresented or suppressed as a consequence of Bd infection. During the warm-wet season, frogs limited Bd infections, recruited putatively beneficial bacteria and returned to pre-infection levels of richness and phylogenetic diversity. In contrast, during the cool-dry season, Bd infections kept increasing through time, and bacterial diversity remained constant. Our findings confirm that infection outcome not only depends on abiotic factors, but also on biotic interactions between hosts and their associated bacterial communities.

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Section: Discussionmentioning

confidence: 94%

Environmental fluctuations and host skin bacteria shift survival advantage between frogs and their fungal pathogen

2016

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“…Thus, host -pathogen interactions are much more complicated than we originally thought (figure 2), and we now must include the possibility that long co-occurrence might have allowed amphibians to develop resistance or tolerance to the pathogens, or that the pathogens have lost virulence. This is borne out by laboratory and field studies showing that prior exposure can increase survival [18,32,96] and that inherent immunogenetic variation in species [17] and populations [97] is correlated with response to disease.…”

Section: Resultsmentioning

confidence: 99%

Overview of chytrid emergence and impacts on amphibians

Lips

2016

Phil. Trans. R. Soc. B

193

169

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One contribution of 18 to a discussion meeting issue 'Tackling emerging fungal threats to animal health, food security and ecosystem resilience'. Chytridiomycosis is an emerging infectious disease of amphibians that affects over 700 species on all continents where amphibians occur. The amphibianchytridiomycosis system is complex, and the response of any amphibian species to chytrid depends on many aspects of the ecology and evolutionary history of the amphibian, the genotype and phenotype of the fungus, and how the biological and physical environment can mediate that interaction. Impacts of chytridiomycosis on amphibians are varied; some species have been driven extinct, populations of others have declined severely, whereas still others have not obviously declined. Understanding patterns and mechanisms of amphibian responses to chytrids is critical for conservation and management. Robust estimates of population numbers are needed to identify species at risk, prioritize taxa for conservation actions, design management strategies for managing populations and species, and to develop effective measures to reduce impacts of chytrids on amphibians.This article is part of the themed issue 'Tackling emerging fungal threats to animal health, food security and ecosystem resilience'.

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“…In assessing the innate immune response, we found that BKA of whole blood increased with larval period. In frogs specifically, BKA predicts susceptibility to disease, specifically chytridiomycosis (Savage et al, ). Our findings indicate that post‐metamorphic amphibians might have a stronger innate immune system if they spend more time as a tadpole.…”

Section: Discussionmentioning

confidence: 99%

Effects of hydroperiod on growth, development, survival and immune defences in a temperate amphibian

et al. 2019

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The many and varied effects of human‐induced environmental change have the potential to threaten animal biodiversity and species abundance. Importantly, human land use and global climate change are predicted to reduce water availability, which might have negative consequences for freshwater organisms. In this study, we tested for an effect of a shortened hydroperiod on larval growth and development, and post‐metamorphic survival and immune function in a temperate frog, Rana pipiens. Animals developing under pond drying conditions metamorphosed at a smaller size and had lower survival after metamorphosis. We found sex‐specific differences in larval period in our fastest drying treatment, with males metamorphosing more quickly than females. Individuals that developed under drying conditions also showed reduced skin swelling after phytohaemagglutinin injection, indicating a compromised immune response. We found support for trade‐offs between growth, development and post‐metamorphic immune function across hydroperiod treatments. Whole blood from animals with shorter larval periods had lower bacterial killing ability, and small‐bodied juveniles had lower antibody titres. Overall, our results indicate that a shortened hydroperiod can affect the rate of larval amphibian growth and development, and might negatively impact the condition of species that rely on freshwater for development. Our work improves understanding of the complex impacts that environmental stressors might have on the health of animal populations. A free Plain Language Summary can be found within the Supporting Information of this article.

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Reduced immune function predicts disease susceptibility in frogs infected with a deadly fungal pathogen

Cited by 33 publications

References 70 publications

Environmental fluctuations and host skin bacteria shift survival advantage between frogs and their fungal pathogen

Environmental fluctuations and host skin bacteria shift survival advantage between frogs and their fungal pathogen

Overview of chytrid emergence and impacts on amphibians

Effects of hydroperiod on growth, development, survival and immune defences in a temperate amphibian

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