Molecular epidemiology and multi-scale drivers of piscine myocarditis virus dispersal in salmon aquaculture.

Abstract

Aquaculture is the fastest-growing animal food-producing sector for human consumption globally. Increasing population size, density, and interconnectivity among farms are expected to markedly increase disease outbreak risks, threatening sector sustainability. Infectious diseases cause around a third of observed mortality in farmed salmon in Norway. Cardiomyopathy syndrome (CMS), caused by piscine myocarditis virus (PMCV), is one of the most frequently detected diseases and often causes high mortality in the late phase of salmon production, compromising fish welfare and causing significant economic losses. Despite its impact, the limited understanding of PMCV dispersal and its drivers hampers effective risk mitigation interventions. To address this, we generated one of the largest genomic datasets for any aquatic viral pathogen, focusing on PMCV collected from Scotland (United Kingdom) and Norway. Combined with detailed metadata, this enabled one of the most comprehensive phylodynamic analyses of a fish virus. Phylodynamic analyses reveal that PMCV likely emerged in farmed salmon concurrent with the global expansion of aquaculture, with a most recent common ancestor around the 1970s-1990s. We identify a distinctive national clustering of virus genomes, reflecting intranational spread interspersed with multiple introductions of distinct PMCV lineages into Scotland. We assess factors influencing virus spread, highlighting the importance of geographic proximity and at-sea farm density, and the possible role of boat connectivity in facilitating long-distance dispersal events. Overall, our study emphasizes the importance of viral genomics in understanding the evolutionary and dispersal dynamics of aquatic pathogens and informs targeted biosecurity strategies to mitigate the growing risk of viral disease in expanding aquaculture systems.