Genetic potential for disease resistance in critically endangered amphibians decimated by chytridiomycosis

Kosch, Tiffany A.; Silva, C. N. S.; Brannelly, Laura A.; Roberts, A. W.; Lau, Quintin; Marantelli, Gerry; Berger, Lee; Skerratt, Lee F.

doi:10.1111/acv.12459

Cited by 41 publications

(46 citation statements)

References 85 publications

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“…In contrast, there appears to be a greater reliance on innate and inflammatory pathways when temperatures are lower, where the greatest number of mortalities were observed. We now have evidence for the importance of the MHC genotypes in amphibian–chytrid resistance (Bataille et al, ; Kosch et al, ; Savage & Zamudio, , ). However, our results indicate that environmental temperature and MHC genotypes must be considered together to fully explain population differences in Bd susceptibility.…”

Section: Discussionmentioning

confidence: 99%

“…Previous amphibian MHC– Bd studies have been primarily focused on MHC class II genotype–survival associations (Bataille et al, ; Savage & Zamudio, , ). More recently, however, specific MHC I alleles have been linked to increased Bd susceptibility (Kosch et al, ). Both classes of MHC genes have been found to be upregulated in the skin during late‐stage infections in frogs (Ellison et al, ; Grogan, Cashins, et al, ; Rosenblum et al, ).…”

Section: Discussionmentioning

confidence: 99%

“…Intriguingly, our data indicate that adaptive immunity, particularly MHC‐related pathways, are thermally sensitive. Given the recent findings for the importance of MHC genotypes in survival against Bd (Bataille et al, ; Kosch et al, ; Savage & Zamudio, , ), it would be valuable to follow this up with an expanded population MHC genotyping and expression study of P. cinereus . Furthermore, in the face of climate change, and as concerns for the spread of the newly discovered chytrid Bsal increase (Stegen et al, ), comparison of salamander functional genomic responses to both chytrid pathogens incorporating thermal variation will be vital to understand how these emergent pathogens may continue to affect amphibian communities globally in the future.…”

Section: Discussionmentioning

confidence: 99%

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Temperature‐mediated shifts in salamander transcriptomic responses to the amphibian‐killing fungus

et al. 2020

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Life processes of ectothermic vertebrates are intimately linked to the temperature of their environment, influencing their metabolism, reproduction, behaviour and immune responses. In amphibians infected by the generalist chytrid pathogen Batrachochytrium dendrobatidis (Bd), host survival, infection prevalence and infection intensity are often temperature‐ and/or seasonally dependent. However, the transcriptional underpinnings of thermal differences in infection responses remain unknown. Measuring the impact of temperature on host responses to infection is a key component for understanding climatic influences on chytrid disease dynamics. The Bd‐responsive gene pathways in frogs are well documented, but our understanding of salamander immune expression profiles during infection with chytrids remains limited. Here we characterize the transcriptomic responses of Plethodon cinereus using RNA sequencing by comparing skin and splenic gene expression of individuals uninfected, succumbing to Bd infection and naturally cleared of Bd infection at three temperatures. We suggest that amphibian temperature‐dependent susceptibility to Bd is probably driven by shifts in expression of the innate and adaptive immune axes. Our study shows increased expression of transcripts associated with inflammation at lower temperatures and a shift towards increased expression of adaptive immune genes, including MHC (major histocompatibility complex), at higher temperatures. In the face of climate change, and as concerns for the spread of emergent chytrid pathogens increase, our results provide important functional genomic resources to help understand how these pathogenic fungi may continue to affect amphibian communities globally in the future.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Temperature‐mediated shifts in salamander transcriptomic responses to the amphibian‐killing fungus

et al. 2020

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“…Our results suggest that management strategies which can reduce the amount of Bd in the environment or the susceptibility of the amphibian will be critical in reducing mortality in epizootic events. Strategies to do so include treatment of amphibians and/or their environment with antifungal compounds (Bosch et al, ), probiotics (Harris et al, ; Kueneman et al, ; Muletz et al, ) and selective breeding for immune‐resistant individuals (Kosch et al, ).…”

Section: Discussionmentioning

confidence: 99%

Fungal disease and temperature alter skin microbiome structure in an experimental salamander system

2019

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Pathogens compete with host microbiomes for space and resources. Their shared environment impacts pathogen-microbiome-host interactions, which can lead to variation in disease outcome. The skin microbiome of red-backed salamanders (Plethodon cinereus) can reduce infection by the pathogen Batrachochytrium dendrobatidis (Bd) at moderate infection loads, with high species richness and high abundance of competitors as putative mechanisms. However, it is unclear if the skin microbiome can reduce epizootic Bd loads across temperatures. We conducted a laboratory experiment to quantify skin microbiome and host responses (P. cinereus: n = 87) to Bd at mimicked epizootic loads across temperatures (13, 17 and 21°C). We quantified skin microbiomes using 16S rRNA gene metabarcoding and identified operational taxonomic units (OTUs) taxonomically similar to culturable bacteria known to kill Bd (anti-Bd OTUs). Prior to pathogen exposure, temperature changed the microbiome (OTU richness decreased by 12% and the abundance of anti-Bd OTUs increased by 18% per degree increase in temperature), but these changes were not predictive of disease outcome. After exposure, Bd changed the microbiome (OTU richness decreased by 0.1% and the abundance of anti-Bd OTUs increased by 0.2% per 1% increase in Bd load) and caused high host mortality across temperatures (35/45: 78%). Temperature indirectly impacted microbiome change and mortality through its direct effect on pathogen load. We did not find support for the microbiome impacting Bd load or host survival. Our research reveals complex host, pathogen, microbiome and environmental interactions to demonstrate that during epizootic events the microbiome will be unlikely to reduce pathogen invasion, even for putatively Bd-resistant species. K E Y W O R D Santifungal, Batrachochytrium dendrobatidis, climate, epidemic, invasion, microbiota, symbiosis

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“…Low genetic diversity can affect fitness and survival, as shown for instance in cheetah, Florida panthers and Alpine ibex (Brambilla et al, 2015;O'Brien et al, 1983O'Brien et al, , 1985Pimm et al, 2006;Reed & Frankham, 2003;Roelke et al, 1993). Loss of genetic diversity at adaptive immune loci is particularly problematic because populations will lack genetic variants conferring disease resistance, in particular infectious diseases, as it has been shown for example in amphibians (Kosch et al, 2019;Savage et al, 2011), Tasmanian devils (Siddle et al, 2007), giant panda (Zhu et al, 2020) and Alpine ibex (Brambilla et al, 2018). However, despite the importance for conservation management, the genetic underpinnings of disease susceptibility are largely unknown in most non-model species (Schoville et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

A robust sequencing assay of a thousand amplicons for the high-throughput population monitoring of Alpine ibex immunogenetics

Kessler

Brambilla

Waldvogel

et al. 2020

Preprint

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Genetic variation is a major factor determining susceptibility to diseases. Polymorphism at the major histocompatibility complex (MHC) and other immune function loci can underlie health and reproductive success of individuals. Endangered species of low population size could be severely compromised to evolve disease resistance due to reduced adaptive variation. A major impediment to screen adaptive genetic variation in wild species is the difficulty to comprehensively genotype immune-related loci based on low input material. Here, we design and validate a targeted amplicon sequencing assay to parallelize the analysis of a thousand loci of the MHC, other immunity-related genes, and genome-wide markers for the assessment of population structure. We apply the approach to Alpine ibex, one of the most successful examples of restoration of a large mammal in Europe. We used 51 whole genome sequenced individuals to select representative target SNPs. We integrated SNP call data from four related species for amplification robustness and genotyped 158 Alpine ibex individuals for validation. We show that the genome-wide markers perform equally well at resolving population structure as RAD-seq or low-coverage genome sequencing datasets with orders of magnitude more markers. The targeted amplicon sequencing assay is robust to >100-fold variation in input DNA quantity and generates useful genotype information from fecal samples. The amplicon marker set also identified recent species hybridization events with domestic goats. The immune loci show unexpectedly high degrees of differentiation within the species. Our assay strategy can realistically be implemented into population genetic surveys of a large range of species.

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Genetic potential for disease resistance in critically endangered amphibians decimated by chytridiomycosis

Abstract: This is the author manuscript accepted for publication and has undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. Please cite this article as

Cited by 41 publications

References 85 publications

Temperature‐mediated shifts in salamander transcriptomic responses to the amphibian‐killing fungus

Temperature‐mediated shifts in salamander transcriptomic responses to the amphibian‐killing fungus

Fungal disease and temperature alter skin microbiome structure in an experimental salamander system

A robust sequencing assay of a thousand amplicons for the high-throughput population monitoring of Alpine ibex immunogenetics

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