Putative resistance and tolerance mechanisms have little impact on disease progression for an emerging salamander pathogen

Abstract

Resistance and tolerance are unique host defence strategies that can limit the impacts of a pathogen on a host. However, for most wildlife–pathogen systems, there are still fundamental uncertainties regarding (a) how changes in resistance and tolerance can affect disease outcomes and (b) the mechanisms underlying resistance and tolerance in host populations. Here, we first compared observed patterns of resistance and tolerance and their effects on disease outcomes among salamander species that are susceptible to infection and mortality from the emerging fungal pathogen Batrachochytrium salamandrivorans (Bsal). We then tested whether two putative mechanisms that contribute to host resistance and tolerance, skin sloughing and skin lesion reduction, predicted reduced Bsal growth rate or increased host survival during infection, respectively. We performed multi‐dose Bsal challenge experiments on four species of Salamandridae found throughout North America. We combined the laboratory experiments with dynamic models and sensitivity analysis to examine how changes in load‐dependent resistance and tolerance functions affected Bsal‐induced mortality risk. Finally, we used our disease model to test whether skin sloughing and lesion reduction predicted variability in infection outcomes not described by Bsal infection intensity. We found that resistance and tolerance differed significantly among salamander species, with the most susceptible species being both less resistance and less tolerant of Bsal infection. Our dynamic model showed that the relative influence of resistance versus tolerance on host survival was species‐dependent—increasing resistance was only more influential than increasing tolerance for the least tolerant species where changes in pathogen load had a threshold‐like effect on host survival. Testing two candidate mechanisms of resistance and tolerance, skin sloughing and lesion reduction, respectively, we found limited support that either of these processes were strong mechanisms of host defence. Our study contributes to a broader understanding of resistance and tolerance in host–pathogen systems by showing that differences in host tolerance can significantly affect whether changes in resistance or tolerance have larger effects on disease outcomes, highlighting the need for species and even population‐specific management approaches that target host defence strategies. A free Plain Language Summary can be found within the Supporting Information of this article.

Evolution of pathogen tolerance and emerging infections: A missing experimental paradigm

“…Conversely, tolerance is easier to estimate where pathogen-specific impacts on measurable host fitness parameters are known. For example, a recent study standardized skin lesion prevention efficacy as an important fitness proxy to estimate tolerance in salamander species to a pathogen Batrachochytrium salamandrivorans that usually infects amphibian skins ( Wilber et al, 2021 ). In contrast, another study used the extent of fin damage caused by ectoparasite Tracheliastes polycolpus (which feeds specifically on and destroys fins) as a proxy in a wild population of cyprinid freshwater fish ( Leuciscus burdigalensis ) ( Mazé-Guilmo et al, 2014 ).…”

Ongoing amphibian trade into the United States threatens salamander biodiversity

“…Amphibian conservationists have been particularly worried about the consequences of Bsal introduction to the United States given the country’s salamander biodiversity. The United States hosts nearly 30% of all salamander species globally (Yap et al 2015), and prospective laboratory studies on native North American amphibians indicate that numerous species are susceptible to lethal Bsal infection (Carter et al 2020, Wilber et al 2021, Gray et al 2022). In light of its potentially large pool of Bsal -susceptible salamander species, the robust amphibian trade into the United States raises serious concerns.…”

Centrifugation is an effective and inexpensive way to determine Batrachochytrium dendrobatidis quantity in water samples with low turbidity

“…Disease models provide us predictive frameworks that can be utilized for both established pathogen outbreaks and with new emerging diseases (e.g. see Briggs et al, 2010;Wilber et al, 2021). Determining the shedding rate of an infectious host, for example, helps us understand and predict disease risk at a population-and community-level.…”