Diversity, evolution, and emergence of fish viruses

Abstract

The production of aquatic animals has more than doubled over the last 50 years and is anticipated to continually increase. While fish are recognized as a valuable and sustainable source of nutrition, particularly in the context of human population growth and climate change, the rapid expansion of aquaculture coincides with the emergence of highly pathogenic viruses that often spread globally through aquacultural practices. Here, we provide an overview of the fish virome and its relevance for disease emergence, with a focus on the insights gained through metagenomic sequencing, noting potential areas for future study. In particular, we describe the diversity and evolution of fish viruses, for which the majority have no known disease associations, and demonstrate how viruses emerge in fish populations, most notably at an expanding domestic-wild interface. We also show how wild fish are a powerful and tractable model system to study virus ecology and evolution more broadly and can be used to identify the major factors that shape vertebrate viromes. Central to this is a process of virus-host co-divergence that proceeds over many millions of years, combined with ongoing cross-species virus transmission.

Keywords: aquaculture; ecology; emerging disease; evolution; fish; virome; virus.

Fig 1

Viral families known to infect fish. (A) Viral sequences on NCBI/GenBank by year of release. (B) Percentage of viral sequences for fish viral families on NCBI/GenBank. (C) Number of viral families on NCBI/GenBank by year of release.

Fig 2

Phylogenetic relationships among notable RNA virus pathogens of fish. Maximum likelihood phylogenies were estimated using amino acid sequence alignments of the RdRp gene using MAAFT (131). The best-fit model of amino acid substitution was estimated with the “ModelFinder Plus” (-m MFP) flag in IQ-TREE (v.1.6.12) (132, 133), and 1,000 bootstrap replicates were used to estimate node support. Circles and labels on the tree tips of fish viruses denote pathogens, while all other fish viruses represent asymptomatic infections. The scale bar represents the number of amino acid substitutions per site. Asterisks denote a bootstrap value of 70% or greater.

Fig 3

Phylogenetic relationships of notable DNA viral pathogens in fish. Maximum likelihood phylogenies were estimated using amino acid sequence alignments of the major capsid protein for the Iridoviridae, Mimiviridae, and Adomaviridae, NS1 protein for the Parvoviridae, E1 protein for the Papillomaviridae, and DNA polymerase for the Poxviridae, and Alloherpesiviridae using MAAFT (131). The best-fit model of amino acid substitution was estimated with the “ModelFinder Plus” (-m MFP) flag in IQ-TREE (v.1.6.12) (132, 133), and 1,000 bootstrap replicates were used to estimate node support. Circles and labels on the tree tips of fish viruses denote pathogens, while all other fish viruses represent asymptomatic infections. The scale bar represents the number of amino acid substitutions per site. Asterisks denote a bootstrap value of 70% or greater.

Fig 4

Interacting biological (blue) and ecological factors (orange) that influence viral disease emergence in aquaculture systems. Viruses are often silently translocated over vast geographic distances to new environments through the international trade of fish eggs, broodstock, wild-sourced larvae, and ornamental fishes. Viruses can enter aquaculture facilities through the international trade or through net-pen cages that attract wild reservoirs (e.g., donor hosts). Following a successful host jump—through the adaptation to a new host species—disease emergence can occur as a result of physiological changes (e.g., stress, nutrition, and immunocompetence) in the recipient host. This process can be exacerbated by low genetic diversity within dense, fish monocultures through selective breeding, inbreeding, and founder effects.