Host evolutionary history and ecology shape virome composition in fishes

Identifying the components of host ecology that promote virus diversity is crucial for our understanding of the drivers of virus evolution and disease emergence. As the most species-rich group of vertebrates that exhibit diverse ecologies, fish provide an ideal model system to study the impacts of host ecology on the composition of their viromes. To better understand the factors that shape virome composition in marine fishes, we characterised the viromes of 23 fish species (19 from this study and four that were sampled previously (Geoghegan et al 2018a)) using unbiased bulk RNA-sequencing (meta-transcriptomics) together with both sequence and protein structural homology searches to identify divergent viruses that often evade characterisation. These data revealed that fish virome composition – that is, viral richness, abundance and diversity – were predominantly shaped by the phylogenetic history of their hosts, as reflected in taxonomic order. In addition, preferred mean water temperature, climate, habitat depth, community diversity and whether fish swim in schools or are solitary were identified as important ecological features that shaped virome diversity and abundance in these fish. Our analysis also identified 25 new virus transcripts that could be assigned to 11 different viral families, including the first fish virus in the Matonaviridae . Other viruses identified fell within the Astroviridae, Picornaviridae, Arenaviridae, Reoviridae, Hepadnaviridae, Paramyxoviridae, Rhabdoviridae, Hantaviridae, Filoviridae and Flaviviridae . Our results provide a better understanding of the ecological determinants of virome diversity and support the view that fish harbour a multitude of viruses, of which the vast majority are undescribed.