Genetic variability and ontogeny predict microbiome structure in a disease-challenged montane amphibian

Rachael E Antwis,Kevin Hopkins,Abigail Pretorius,Ché Weldon,Michael D Wood,Graeme Fox,Xavier A Harrison,Sarah M Griffiths,Richard F Preziosi

doi:10.1038/s41396-018-0167-0

Abstract

Amphibian populations worldwide are at risk of extinction from infectious diseases, including chytridiomycosis caused by the fungal pathogen Batrachochytrium dendrobatidis (Bd). Amphibian cutaneous microbiomes interact with Bd and can confer protective benefits to the host. The composition of the microbiome itself is influenced by many environment- and host-related factors. However, little is known about the interacting effects of host population structure, genetic variation and developmental stage on microbiome composition and Bd prevalence across multiple sites. Here we explore these questions in Amietia hymenopus, a disease-affected frog in southern Africa. We use microsatellite genotyping and 16S amplicon sequencing to show that the microbiome associated with tadpole mouthparts is structured spatially, and is influenced by host genotype and developmental stage. We observed strong genetic structure in host populations based on rivers and geographic distances, but this did not correspond to spatial patterns in microbiome composition. These results indicate that demographic and host genetic factors affect microbiome composition within sites, but different factors are responsible for host population structure and microbiome structure at the between-site level. Our results help to elucidate complex within- and among- population drivers of microbiome structure in amphibian populations. That there is a genetic basis to microbiome composition in amphibians could help to inform amphibian conservation efforts against infectious diseases.

Highlights

IntroductionMulticellular organisms act as hosts to a diverse suite of bacterial communities, collectively referred to as the microbiome
Despite a lack of similarity between host population genetic structure and site-level microbiome structure, genetic distance among hosts is still significantly correlated with associated microbial community dissimilarity when controlling for geographic distance
We have shown that the microbiome composition of amphibians is determined by genetic and ontogenetic variation, as well as geographic site, indicating within and among population predictors of microbiome diversity

Summary

Introduction

Multicellular organisms act as hosts to a diverse suite of bacterial communities, collectively referred to as the microbiome. Recent research across multiple taxa has highlighted that these bacterial communities perform beneficial functions for the host, including protection from infectious pathogens [1,2,3]. Despite the importance of symbiotic relationships between microbes and their hosts, a comprehensive understanding of factors that influence the diversity and composition of the microbiome, for non-human animals, is lacking. Studying factors that determine variation in the distribution of bacterial symbionts at both the individual and landscape scale is crucial for understanding how individual susceptibility to pathogens varies within and among populations

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