Abstract
Microbiome-pathogen interactions are increasingly recognized as an important element of host immunity. While these host-level interactions will have consequences for community disease dynamics, the factors which influence host microbiomes at larger scales are poorly understood. We here describe landscape-scale pathogen-microbiome associations within the context of post-epizootic amphibian chytridiomycosis, a disease caused by the panzootic chytrid fungus Batrachochytrium dendrobatidis. We undertook a survey of Neotropical amphibians across altitudinal gradients in Ecuador ~30years following the observed amphibian declines and collected skin swab-samples which were metabarcoded using both fungal (ITS-2) and bacterial (r16S) amplicons. The data revealed marked variation in patterns of both B.dendrobatidis infection and microbiome structure that are associated with host life history. Stream breeding amphibians were most likely to be infected with B.dendrobatidis. This increased probability of infection was further associated with increased abundance and diversity of non-Batrachochytrium chytrid fungi in the skin and environmental microbiome. We also show that increased alpha diversity and the relative abundance of fungi are lower in the skin microbiome of adult stream amphibians compared to adult pond-breeding amphibians, an association not seen for bacteria. Finally, stream tadpoles exhibit lower proportions of predicted protective microbial taxa than pond tadpoles, suggesting reduced biotic resistance. Our analyses show that host breeding ecology strongly shapes pathogen-microbiome associations at a landscape scale, a trait that may influence resilience in the face of emerging infectious diseases.
Highlights
The spread of invasive pathogens linked to increasing global connectivity is a major driver of biodiversity losses worldwide and the attendant attrition of ecosystem functions (Crowl et al, 2008; Thakur et al, 2019)
Over 30 years following epizootic declines caused by chytridiomycosis in Neotropical amphibian populations we find that the presence of B. dendrobatidis, as well as novel undescribed native chytrids, are strongly associated with stream-breeding amphibian communities
Our data show that amphibian life history traits modify both host bacterial and fungal microbiomes, and susceptibility to infection with Batrachochytrium dendrobatidis
Summary
The spread of invasive pathogens linked to increasing global connectivity is a major driver of biodiversity losses worldwide and the attendant attrition of ecosystem functions (Crowl et al, 2008; Thakur et al, 2019). The spread and establishment of a pathogen during an initial epizootic outbreak phase does not guarantee naturalization within a host system (Anderson & May, 1986) and, following an epizootic, the long-term persistence of a pathogen is governed by a combination of biotic and abiotic factors (Hawley & Altizer, 2011) Understanding these factors is a critical step for informing disease mitigation strategies as well as assessing the risk of invasion to naïve communities (Beukema et al, 2018; Canessa et al, 2020). Observed heterogeneity in disease susceptibility has been attributed to a range of biotic and abiotic factors that includes the intrinsic variation in resilience of hosts to B. dendrobatidis that is lent by immune-mechanisms (Cohen et al, 2017; Woodhams et al, 2006, 2014) This local web of interactions comprises the realized niche of B. dendrobatidis and determines whether the pathogen thrives or dies (Hawley & Altizer, 2011). We (i) assess the relative importance of abiotic (elevation) and biotic (host breeding mode and life stage) as factors in determining the presence of B. dendrobatidis; (ii) correlate domain-level host microbiome composition with factors predicting B. dendrobatidis presence; and (iii) determine the presence and diversity of non-Batrachochytrium chytrid fungi in relation to factors associated with B. dendrobatidis presence
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