Aquaculture mediates global transmission of a viral pathogen to wild salmon.

Gideon J Mordecai,Amy Tabata,Kristina M Miller,Jessica M Caleta,Tobi J Ming,Arthur L Bass,Emiliano Di Cicco,Amy K Teffer,Shaorong Li,Angela D Schulze,Brad R Jones,Jeffrey B Joy,Karia H Kaukinen,Andrew W Bateman

doi:10.1126/sciadv.abe2592

Abstract

Global expansion of aquaculture and agriculture facilitates disease emergence and catalyzes transmission to sympatric wildlife populations. The health of wild salmon stocks critically concerns Indigenous peoples, commercial and recreational fishers, and the general public. Despite potential impact of viral pathogens such as Piscine orthoreovirus-1 (PRV-1) on endangered wild salmon populations, their epidemiology in wild fish populations remains obscure, as does the role of aquaculture in global and local spread. Our phylogeographic analyses of PRV-1 suggest that development of Atlantic salmon aquaculture facilitated spread from Europe to the North and South East Pacific. Phylogenetic analysis and reverse transcription polymerase chain reaction surveillance further illuminate the circumstances of emergence of PRV-1 in the North East Pacific and provide strong evidence for Atlantic salmon aquaculture as a source of infection in wild Pacific salmon. PRV-1 is now an important infectious agent in critically endangered wild Pacific salmon populations, fueled by aquacultural transmission.

Highlights

Pacific salmon (Oncorhynchus spp.) are foundation species, essential for transporting nutrients and energy between aquatic and terrestrial environments [1]
We explored the temporal signal in the sequence data using root-to-tip regression, revealing that Piscine orthoreovirus (PRV)-1a in the North East (NE) Pacific is evolving in a clocklike manner, with genetic diversity accruing proportional to time
Estimated divergence of PRV-1a and PRV-1b in 1942 [95% highest posterior density (HPD) interval, 1908–1968; Fig. 1 and table S1] precedes the 1970 advent of marine net-pen salmon aquaculture in Norway [47], suggesting that both substrains were either a natural part of wild Atlantic salmon populations or they diverged during the development of trout farming in Norway [47]

Summary

Introduction

Pacific salmon (Oncorhynchus spp.) are foundation species, essential for transporting nutrients and energy between aquatic and terrestrial environments [1]. Similarity of emerging infectious agents in the Pacific Ocean with those associated with Atlantic salmon in Europe [19, 20] suggests that these importations may be a source of transmission. We more than double the number of available full PRV-1 genomes and use epidemiological and phylogenetic methods to test hypotheses concerning the global spread of PRV-1 as well as transmission of PRV-1 between farmed Atlantic and wild salmon in the NE Pacific.

Results

Conclusion