Environmental heterogeneity is known to modulate the interactions between pathogens and hosts. However, the impact of environmental heterogeneity on the structure of host-associated microbial communities, and how these communities respond to pathogenic exposure remain poorly understood. Here we use an experimental framework to probe the links between environmental heterogeneity, skin microbiome structure and infection by the emerging pathogen Ranavirus in a vertebrate host, the European common frog (Rana temporaria). We provide evidence that environmental complexity directly influences the diversity and structure of the host skin microbiome, and that more diverse microbiomes are more resistant to perturbation associated with exposure to Ranavirus. Our data also indicate that host microbiome diversity covaries with survival following exposure to Ranavirus. Our study highlights the importance of extrinsic factors in driving host-pathogen dynamics in vertebrate hosts, and suggests that environment-mediated variation in the structure of the host microbiome may covary with observed differences in host susceptibility to disease in the wild.

Infectious diseases can influence the life history strategy of their hosts and such influences subsequently impact the demography of infected populations, reducing viability independently of increased mortality or morbidity. Amphibians are the most threatened group of vertebrates and emerging infectious diseases play a large role in their population declines. Viruses of genus Ranavirus are responsible for one of the deadliest of these diseases. To date no work has evaluated the impact of ranaviruses on host life-history post metamorphosis or population demographic structure at the individual level. In this study, we used skeletochronology and morphology to evaluate the impact of ranaviruses on the demography of populations of European common frog (Rana temporaria) in the United Kingdom. We compared ecologically similar populations that differed only in their historical presence or absence of ranaviral disease. Our results suggest that ranaviruses are associated with shifts in the age structure of infected populations, potentially caused by increased adult mortality and associated shifts in the life history of younger age classes. Population projection models indicate that such age truncation could heighten the vulnerability of frog populations to stochastic environmental challenges. Our individual level data provide further compelling evidence that the emergence of infectious diseases can alter host demography, subsequently increasing population vulnerability to additional stressors.