Abstract

Infectious hematopoietic necrosis (IHN)—a highly lethal infectious salmonid disease—has caused substantial economic losses in the European production of rainbow trout (Oncorhynchus mykiss) since the late 1980s. The causal agent of IHN is the IHN virus (IHNV) introduced from overseas. However, until today, its phylogeographic spread in Europe remains poorly understood. We therefore sought to elucidate this unresolved topic by using the largest ever compiled dataset of European IHNV isolates (E isolates) (193 GenBank E isolates and 100 isolates from this study) for the complete glycoprotein (G) gene sequence. Our results clearly revealed that the active trout trade has left its traces in the E phylogeny. For example, the spread by trade of IHNV-infected trout was apparently the cause for the exposure of the E lineage to different local scenarios of selection and genetic drift, and therefore has led to the split of this lineage into various subordinated lineages. Accordingly, we also found evidence for E isolates being mixed Europe-wide by cross-border introduction events. Moreover, there were indications that this propagation of the E lineage within Europe corresponded with an extensive and rapid spread event, already during or shortly after its formation. Finally, in accordance with the high substitution rate of IHNV determined by previous studies, our dataset indicates that the mean period of occurrence of a single E haplotype is typically not longer than one calendar year.

Highlights

  • The economic efficiency of European rainbow trout (Oncorhynchus mykiss) aquaculture is threatened by a highly lethal fish disease, infectious hematopoietic necrosis (IHN) [1], among many other diseases [1]

  • Our underlying idea is that even a single delivery of infectious hematopoietic necrosis virus (IHNV)-infected trout can cause a hard polytomy, as it can lead to the spread of one IHNV haplotype to various European regions at the same time

  • It could be assumed that this trade-mediated spread has led to the spread of IHNV-infected trout, resulting in the split of the E lineage into a variety of subordinated lineages caused by different local scenarios of selection and genetic drift [26]

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Summary

Introduction

The economic efficiency of European rainbow trout (Oncorhynchus mykiss) aquaculture is threatened by a highly lethal fish disease, infectious hematopoietic necrosis (IHN) [1], among many other diseases [1]. This assumption is based on phylogeographic studies [8], and on the fact that IHN outbreaks were restricted to this area until as late as the late 1960s. We used both a phylogenetic tree and a network method, gene phylogenies of a virus are usually represented only by a rooted bifurcating tree for simplicity This simplification, can imply the risk of unresolved conflicting branching patterns, as a bifurcation algorithm does not permit the correct phylogenetic resolution of a hard polytomy (a multiple, simultaneous divergence event) [26, 27]. Our underlying idea is that even a single delivery of IHNV-infected trout can cause a hard polytomy, as it can lead to the spread of one IHNV haplotype (or very closely related haplotypes) to various European regions at the same time

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