Endemic Lineages of Batrachochytrium dendrobatidis Are Associated With Reduced Chytridiomycosis-Induced Mortality in Amphibians: Evidence From a Meta-Analysis of Experimental Infection Studies

Abstract

Emerging infectious wildlife diseases have caused devastating declines, particularly when pathogens have been introduced in naïve host populations. The outcome of disease emergence in any host population will be dictated by a series of factors including pathogen virulence, host susceptibility, and prior opportunity for coevolution between hosts and pathogens. Historical coevolution can lead to increased resistance in hosts and/or reduced virulence in endemic pathogens that allows stable persistence of host and pathogen populations. Adaptive coevolution may also occur on relatively short time scales following introduction of a novel pathogen. Here, we performed a meta-analysis of multi-strain Batrachochytrium dendrobatidis (Bd) infection experiments to test whether: (1) amphibian hosts exhibit lower mortality rates when infected with strains belonging to endemic Bd lineages relative to the Global Panzootic Lineage (Bd-GPL), hypothetically owing to long co-evolutionary histories between endemic Bd lineages and their amphibian hosts; and (2) amphibians exhibit lower mortality rates when infected with local Bd-GPL strains compared with non-local Bd-GPL strains, hypothetically owing to recent selection for tolerance or resistance to local Bd-GPL strains. We found that in a majority of cases, amphibians in endemic Bd treatments experienced reduced mortality relative to those in Bd-GPL treatments. Hosts presumed to have historically coexisted with endemic Bd did not show reduced mortality to Bd-GPL compared with hosts that have not historically coexisted with endemic Bd. Finally, we detected no overall difference in amphibian mortality between local and non-local Bd-GPL treatments. Taken together, our results suggest that long-term historical coexistence is associated with less disease-induced mortality potentially due to hypovirulence in endemic Bd lineages, and that more recent coexistence between amphibians and Bd-GPL has not yet resulted in reduced host susceptibility or pathogen virulence. This corroborates previous findings that Bd-GPL introduced via the global amphibian trade has a high capacity for causing disease-induced mortality.

Major Histocompatibility Complex Variation and Haplotype Associated Survival in Response to Experimental Infection of Two Bd-GPL Strains Along a Latitudinal Gradient

“…The results obtained, where some haplotypes seem to be more susceptible to the UK-strain than to the Swedish-strain, suggest that southern populations have been coexisting with the Swedish-strain for a longer time, resulting in a reduced host susceptibility or pathogen virulence. Our result is not in concordance with what was found in the Belasen et al (2022) meta-analysis review, where hosts presumed to have historically coexisted with endemic Bd did not show reduced mortality when exposed to Bd-GPL treatments compared with host that have not historically coexisted with endemic Bd; but like they hypothesized, endemic Bd lineages (Bd-GPL strain from Sweden) seems to pose a lower threat to amphibian species than Bd-GPL from UK. Also, Belasen et al (2022) performed a separate analysis comparing local Bd-GPL to non-local GPL strains and did not find a significant difference.…”

“…Our result is not in concordance with what was found in the Belasen et al (2022) meta-analysis review, where hosts presumed to have historically coexisted with endemic Bd did not show reduced mortality when exposed to Bd-GPL treatments compared with host that have not historically coexisted with endemic Bd; but like they hypothesized, endemic Bd lineages (Bd-GPL strain from Sweden) seems to pose a lower threat to amphibian species than Bd-GPL from UK. Also, Belasen et al (2022) performed a separate analysis comparing local Bd-GPL to non-local GPL strains and did not find a significant difference. In any case, our findings highlight the importance of host-and pathogen-dependent factors in determining overall infection virulence.…”

Novel chytrid pathogen variants and the global amphibian pet trade

“…Instead, the hypervirulence of the ancestral BdAsia‐1 lineage was driven by the evolution of enhanced resistance and tolerance mechanisms in their amphibian hosts (Fu & Waldman, 2019). Our results stand in stark contrast to the hypothesis that endemic Bd strains evolve to be hypovirulent to their hosts (Belasen et al., 2022). Because B. orientalis does not clear itself of Bd, but is tolerant of it, carrying low infection loads without showing clinical signs of disease (Bataille et al., 2013), this host species may be especially likely to spread infection to other species.…”

Major Emerging Fungal Diseases of Reptiles and Amphibians

“…Bd can be classified according to lineages, including the very high pathogenic Bd -GPL (global pandemic lineage) and endemic lineages, including Bd -Cape, Bd -Brazil, Bd -Asia, and Bd -CH [ 115 ]. This classification is constantly evolving as new lineages and genotypes are being discovered, including recent evidence of hybridization [ 116 , 117 ].…”