Drivers underpinning heterogeneity in host-pathogen systems

Abstract

The amphibian-infecting chytrid fungi, Batrachochytrium dendrobatidis (Bd) and Batrachochytrium salamandrivorans (Bsal) cause the disease chytridiomycosis and are major agents of global amphibian decline. Despite catastrophic species loss associated with outbreaks of these pathogens, there is within- and between-species heterogeneity in susceptibility to infection, of which our understanding is limited. In this thesis, I investigate the key factors underpinning disease outcome in amphibians. In particular, I focus on the importance of host microbial ecology and whether defensive or synergistic microbe-pathogen relationships shape the host response to infection. In my first data chapter, I show that in wild midwife toad (Alytes obstetricans) populations exhibiting enzootic or epizootic Bd disease dynamics, there is no association between pathogen genetics and epidemiological trends. Meanwhile, I demonstrate strong associations between the host microbiome and disease outcome, with reduced bacterial diversity and differences in community composition in epizootic versus enzootic populations. I further demonstrate that the host skin microbiome differs profoundly based on life stage with larvae and metamorphs exhibiting different bacterial community composition and sharing relatively few microbial taxa. In the following chapter, I begin to disentangle microbe-mediated protection from pathogen-induced disruption of the microbiome by showing that Bsal-induced mortality is associated with microbiome perturbation in two amphibian host species. I further show that transitioning from the wild to captivity results in changes in bacterial and fungal community composition and reduced diversity of the amphibian skin microbiome. In my final chapter, I reveal that skin microbial community structure is linked to mucosal metabolome composition in wild A. obstetricans. In addition, I uncover microbe-metabolite associations linked to population-level disease outcomes. Overall, this thesis exposes some of the key factors driving chytridiomycosis disease dynamics and demonstrates that amphibian skin-associated microbes play an important role in shaping the host response to infection.