Exposure to Corticosterone Affects Host Resistance, but Not Tolerance, to an Emerging Fungal Pathogen

Julie Murone,Matthew D Venesky,Joseph A Demarchi,Matthew C Fisher

doi:10.1371/journal.pone.0163736

Abstract

Host responses to pathogens include defenses that reduce infection burden (i.e., resistance) and traits that reduce the fitness consequences of an infection (i.e., tolerance). Resistance and tolerance are affected by an organism's physiological status. Corticosterone (“CORT”) is a hormone that is associated with the regulation of many physiological processes, including metabolism and reproduction. Because of its role in the stress response, CORT is also considered the primary vertebrate stress hormone. When secreted at high levels, CORT is generally thought to be immunosuppressive. Despite the known association between stress and disease resistance in domesticated organisms, it is unclear whether these associations are ecologically and evolutionary relevant in wildlife species. We conducted a 3x3 fully crossed experiment in which we exposed American toads (Anaxyrus [Bufo] americanus) to one of three levels of exogenous CORT (no CORT, low CORT, or high CORT) and then to either low or high doses of the pathogenic chytrid fungus Batrachochytrium dendrobatidis (“Bd”) or a sham exposure treatment. We assessed Bd infection levels and tested how CORT and Bd affected toad resistance, tolerance, and mortality. Exposure to the high CORT treatment significantly elevated CORT release in toads; however, there was no difference between toads given no CORT or low CORT. Exposure to CORT and Bd each increased toad mortality, but they did not interact to affect mortality. Toads that were exposed to CORT had higher Bd resistance than toads exposed to ethanol controls/low CORT, a pattern opposite that of most studies on domesticated animals. Exposure to CORT did not affect toad tolerance to Bd. Collectively, these results show that physiological stressors can alter a host’s response to a pathogen, but that the outcome might not be straightforward. Future studies that inhibit CORT secretion are needed to better our understanding of the relationship between stress physiology and disease resistance and tolerance in wild vertebrates.

Highlights

Hosts responses to pathogens can be broken into two strategies: those that prevent pathogen colonization or reduce infection burden and those that reduce the fitness consequences of an infection (i.e., [1, 2])
Irrespective of their CORT treatment, toads that were exposed to Batrachochytrium dendrobatidis (Bd) had higher mortality (~33% in the low Bd treatment and ~37% in the high Bd treatment compared to non-exposed toads (~6%)
Our fully factorial laboratory experiment using field-collected American toads (Anaxyrus [Bufo] americanus) exposed to physiologically relevant doses of CORT and the pathogenic chytrid fungus revealed that CORT can mediate an outcome of infectious diseases

Summary

Introduction

Hosts responses to pathogens can be broken into two strategies: those that prevent pathogen colonization or reduce infection burden (i.e., resistance) and those that reduce the fitness consequences of an infection (i.e., [1, 2]). Resistance reduces host infection burden and can thereby. Host resistance imposes negative selection pressures on pathogens, which can potentially increase their virulence within a population [3]. Tolerance responses mitigate the fitness consequences association with an infection (e.g., reducing self-damage from immune responses). In contrast to resistance responses, tolerance responses do not reduce or eliminate pathogen infection burdens and are hypothesized to increase pathogen prevalence within a host population while having neutral or positive selection pressures on pathogen virulence (but see [3, 4]). Host genotypes vary naturally in their resistance and tolerance to infection, these responses are often mediated by environmental conditions in which hosts and pathogens interact (reviewed in [5]). Host traits such as sex [6], age/developmental stage [7], nutritional condition [8], and physiological state [9] are known to affect host immunocompetence and their resistance and tolerance to pathogens

Methods

Results

Conclusion