Aquaculture mediates global transmission of a viral pathogen to wild salmon

Our recently published paper: Aquaculture mediates global transmission of a viral pathogen to wild salmon[1] provides new information regarding pathogen spillover from salmon farms to wild Pacific salmon. We’ve outlined a summary of our findings in a news release, below.

In short, our findings strongly suggest that open-net aquaculture has introduced a non-native infectious agent, Piscine orthoreovirus (PRV), to B.C. Now that it is here, PRV is exceedingly common on salmon farms, and viral spillover to wild salmon occurs.

A scientific, peer-reviewed research process underpins these new findings.

The transfer of pathogens and disease from salmon farms is of significant concern for B.C.’s wild salmon but is very difficult to assess. Prior to our study, there was limited data to make firm conclusions about the transmission of viruses from salmon farms to wild salmon.

As a result, the issue is contentious, with industry highlighting points that suggest the risk is insignificant, and conservation-oriented groups focusing on perceived substantial risks. In this context, there has been much debate about the origin of PRV, and whether it is transmitted from farmed to wild salmon. Our study looked at the genetic history of PRV, which is present in both wild and farmed salmon, to see if its origin and transmission history could be determined.

Our research applied the science of pathogen evolution, using viral genome sequencing, to trace the paths of different viral lineages. Our study sequenced 86 complete PRV genomes (specifically the relevant PRV-1 strain) and conducted analyses on the resulting data, plus existing genome sequences from around the world; this represents the most comprehensive study on PRV evolution and transmission performed to date.

One of the primary points used in attempts to discredit scientific findings related to PRV introduction and transmission in B.C. is a putative detection of PRV from one archival sample, collected in 1977 from one fish (a steelhead). This has been used by some as evidence that this virus was present in B.C. waters long before open-net pen salmon aquaculture began in B.C.  As we have noted in our paper and in the summary below, however, this finding remains suspect.

Irrespective of PRV’s presence in 1977, a primary take-away of our work is that open-net salmon aquaculture can introduce non-native infectious agents to new environments. In the case of PRV, we show that this has happened multiple times around the world, and at least once in the Salish Sea.

 

Our Science Advances paper offers several key findings:

  • The analysis clearly showed that the lineage of PRV in the North East Pacific originates from the North East Atlantic. This agrees with previous findings[2], including a recent study from a different group of B.C. and Washington scientists (including industry scientists) in 2020[3].
  • Our data indicated that the ancestor of the PRV lineage currently found in both farmed and wild salmon in B.C. arrived some time between 1981 and 1997, approximately 30 years ago.
  • Two lines of evidence strongly suggested transmission of PRV between farmed and wild salmon:
    • Genomic data show that B.C.’s farmed and wild salmon share multiple viral variants.
    • PRV infection in B.C. juvenile free-ranging Chinook salmon declined with distance from active salmon farms.

Changes in the viral genome over time contain information about the past population size of the virus. Our analysis indicates a growth in the number of PRV infections in the NE Pacific over the last decades, a pattern that aligns with regional growth in aquaculture, and high rates of PRV infection in farms. This, paired with our estimated arrival date for the currently circulating PRV lineage (consistent with the timing of Atlantic salmon egg imports from Europe for salmon farming), suggests that widespread PRV infection in wild B.C. Pacific salmon is a relatively recent phenomenon, coincident with the growth of salmon farming in B.C.

There have been several other PRV phylogenetic studies, but none as comprehensive as ours. The 1977 PRV sample is addressed in the paper:

The source and age of PRV in the North East (NE) Pacific is contentious[2,3], with very low-load putative detections (unverified by sequencing) as long ago as 1977[4]. These detections are considered putative findings only, and to validate them, a peer-reviewed study would need to sequence archival PRV from 1977 and should include sufficient controls to screen out contaminants.

Our assessment of the 1977 sample is congruent with a 2015 DFO CSAS report, which labels the 1977 detection as “suspect” [5]. As we state in our paper, we welcome further, peer-reviewed research on the putative detection in the archival sample.  We propose that the phylogenetic framework developed by ourselves and other groups will enable validation of sequences to determine if they truly were amplified from archival materials, since older sequences should either be ancestral to more recent PRV sequences found in the NE Pacific, or differ in sequence if they were the result of a separate, earlier introduction.  Instead, the putative 1977 sequence currently lacks peer-reviewed documentation and is identical to modern sequences – a possible indication of sample contamination.

Further, our genomic epidemiological investigation found evidence for other global transmission events, including a more recent introduction of the virus to the NE Pacific detected in escaped Atlantic salmon in Washington state, which we propose was likely introduced from Icelandic eggs[6].

Regardless, there is wide consensus that the virus originates from the North Atlantic. The date of introduction does not determine the risk posed at the present day. As noted at the outset, the important evidence at hand strongly suggests that open-net aquaculture has been allowed to introduce non-native infectious agents to B.C. Our study shows that one of these agents, PRV, is exceedingly common on salmon farms, and that viral spillover to wild salmon occurs.

We call attention to the disease risk posed to wild salmon in B.C.: A Norwegian lab challenge in Atlantic salmon found a B.C. isolate of PRV to cause lesions consistent with the disease Heart and Skeletal Muscle Inflammation (HSMI)[7], corroborating reports of heart lesions and full-blown HSMI in B.C. lab[8] and field[9] studies, respectively. Crucially, PRV has also been tightly associated with Jaundice/Anemia disease in both farmed and wild Chinook salmon[10,11].

The risk to wild salmon is real.

 

Gideon Mordecai
UBC & PSF

Andrew Bateman
PSF & UofT

Emiliano Di Cicco
PSF

 

References

[1]    G. J. Mordecai, K. M. Miller, A. L. Bass, A. W. Bateman, A. K. Teffer, J. M. Caleta, E. Di Cicco, A. D. Schulze, K. H. Kaukinen, S. Li, A. Tabata, B. R. Jones, T. J. Ming, J. B. Joy, Sci Adv 2021, 7, DOI 10.1126/sciadv.abe2592.

[2]    M. J. T. Kibenge, T. Iwamoto, Y. Wang, A. Morton, M. G. Godoy, F. S. B. Kibenge, Virol. J. 2013, 10, 230.

[3]    A. Siah, B. R. Breyta, K. I. Warheit, N. Gagne, M. K. Purcell, D. Morrison, J. F. F. Powell, S. C. Johnson, Virus Evol 2020, DOI 10.1093/ve/veaa054.

[4]    G. D. Marty, D. B. Morrison, J. Bidulka, T. Joseph, A. Siah, J. Fish Dis. 2015, 38, 713.

[5]    Canadian Science Advisory Secretariat, n.d.

[6]    M. J. T. Kibenge, Y. Wang, N. Gayeski, A. Morton, K. Beardslee, B. McMillan, F. S. B. Kibenge, Virol. J. 2019, 16, 41.

[7]    Ø. Wessel, E. F. Hansen, M. K. Dahle, M. Alarcon, N. A. Vatne, I. B. Nyman, K. B. Soleim, K. Dhamotharan, G. Timmerhaus, T. Markussen, M. Lund, H. Aanes, M. Devold, M. Inami, M. Løvoll, E. Rimstad, Pathogens 2020, 9, 1050.

[8]    M. P. Polinski, G. D. Marty, H. N. Snyman, K. A. Garver, Sci. Rep. 2019, 9, 3297.

[9]    E. Di Cicco, H. W. Ferguson, A. D. Schulze, K. H. Kaukinen, S. Li, R. Vanderstichel, Ø. Wessel, E. Rimstad, I. A. Gardner, K. L. Hammell, K. M. Miller, PLoS One 2017, 12, e0171471.

[10]  E. Di Cicco, H. W. Ferguson, K. H. Kaukinen, A. D. Schulze, S. Li, A. Tabata, O. P. Günther, G. Mordecai, C. A. Suttle, K. M. Miller, FACETS 2018, 3, 599.

[11]  Y. Wang, The Physiological Associations between Infectious Agents and Migrating Juvenile Chinook Salmon (Oncorhynchus Tshawytscha), University of British Columbia, 2018.