Gene expression differs in susceptible and resistant amphibians exposed to Batrachochytrium dendrobatidis

Author:

Eskew Evan A.12ORCID,Shock Barbara C.34,LaDouceur Elise E. B.5,Keel Kevin4,Miller Michael R.6,Foley Janet E.7,Todd Brian D.8

Affiliation:

1. Graduate Group in Ecology, University of California, Davis, One Shields Avenue, Davis, CA 95616, USA

2. EcoHealth Alliance, 460 West 34th Street – 17th Floor, New York, NY 10001, USA

3. Department of Biology, Lincoln Memorial University, 6965 Cumberland Gap Parkway, Harrogate, TN 37752, USA

4. Department of Pathology, Microbiology, and Immunology, School of Veterinary Medicine, University of California, Davis, One Shields Avenue, Davis, CA 95616, USA

5. Northwest ZooPath, 654 West Main Street, Monroe, WA 98272, USA

6. Department of Animal Science, University of California, Davis, One Shields Avenue, Davis, CA 95616, USA

7. Department of Medicine and Epidemiology, School of Veterinary Medicine, University of California, Davis, One Shields Avenue, Davis, CA 95616, USA

8. Department of Wildlife, Fish, and Conservation Biology, University of California, Davis, One Shields Avenue, Davis, CA 95616, USA

Abstract

Chytridiomycosis, the disease caused by the fungal pathogen Batrachochytrium dendrobatidis ( Bd ), has devastated global amphibian biodiversity. Nevertheless, some hosts avoid disease after Bd exposure even as others experience near-complete extirpation. It remains unclear whether the amphibian adaptive immune system plays a role in Bd defence. Here, we describe gene expression in two host species—one susceptible to chytridiomycosis and one resistant—following exposure to two Bd isolates that differ in virulence. Susceptible wood frogs ( Rana sylvatica ) had high infection loads and mortality when exposed to the more virulent Bd isolate but lower infection loads and no fatal disease when exposed to the less virulent isolate. Resistant American bullfrogs ( R. catesbeiana ) had high survival across treatments and rapidly cleared Bd infection or avoided infection entirely. We found widespread upregulation of adaptive immune genes and downregulation of important metabolic and cellular maintenance components in wood frogs after Bd exposure, whereas American bullfrogs showed little gene expression change and no evidence of an adaptive immune response. Wood frog responses suggest that adaptive immune defences may be ineffective against virulent Bd isolates that can cause rapid physiological dysfunction. By contrast, American bullfrogs exhibited robust resistance to Bd that is likely attributable, at least in part, to their continued upkeep of metabolic and skin integrity pathways as well as greater antimicrobial peptide expression compared to wood frogs, regardless of exposure. Greater understanding of these defences will ultimately help conservationists manage chytridiomycosis.

Funder

National Science Foundation

Publisher

The Royal Society

Subject

Multidisciplinary

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