Atlantic salmon populations invaded by farmed escapees: quantifying genetic introgression with a Bayesian approach and SNPs

Abstract Norwegian aquaculture has grown from its pioneering days in the 1970s to be a major industry. It is primarily based on culturing Atlantic salmon and rainbow trout and has the potential to influence the surrounding environment and wild populations. To evaluate these potential hazards, the Institute of Marine Research initiated a risk assessment of Norwegian salmon farming in 2011. This assessment has been repeated annually since. Here, we describe the background, methods and limitations of the risk assessment for the following hazards: genetic introgression of farmed salmon in wild populations, regulatory effects of salmon lice and viral diseases on wild salmonid populations, local and regional impact of nutrients and organic load. The main findings are as follows: (i) 21 of the 34 wild salmon populations investigated indicated moderate-to-high risk for genetic introgression from farmed escaped salmon. (ii) of 109 stations investigated along the Norwegian coast for salmon lice infection, 27 indicated moderate-to-high likelihood of mortality for salmon smolts while 67 stations indicated moderate-to-high mortality of wild sea trout. (iii) Viral disease outbreaks (pancreas disease, infectious pancreatic necrosis, heart and skeletal muscle inflammation, and cardiomyopathy syndrome) in Norwegian salmon farming suggest extensive release of viruses in many areas. However, screening of wild salmonids revealed low to very low prevalence of the causal viruses. (iv) From ∼500 yearly investigations of local organic loading under fish farms, only 2% of them displayed unacceptable conditions in 2013. The risk of eutrophication and organic load beyond the production area of the farm is considered low. Despite several limitations, especially limited monitoring data, this work represents one of the world’s first risk assessment of aquaculture. This has provided the Norwegian government with the basis upon which to take decisions for further development of the Norwegian aquaculture industry.

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Widespread genetic introgression of escaped farmed Atlantic salmon in wild salmon populations

ICES Journal of Marine Science ◽

10.1093/icesjms/fsw121 ◽

2016 ◽

Vol 73 (10) ◽

pp. 2488-2498 ◽

Cited By ~ 64

Author(s):

Sten Karlsson ◽

Ola H. Diserud ◽

Peder Fiske ◽

Kjetil Hindar ◽

Keyword(s):

Atlantic Salmon ◽

Molecular Genetic ◽

Genetic Introgression ◽

Wild Salmon ◽

Farmed Salmon ◽

Geographical Regions ◽

Average Proportion ◽

Population Sizes ◽

Farmed Atlantic Salmon ◽

High Level

Abstract Farmed Atlantic salmon (Salmo salar) escape from net pens and enter rivers to spawn, potentially resulting in genetic introgression and reduced fitness of wild salmon. Here, we quantify genetic introgression of farmed to wild salmon, using molecular genetic markers, in populations from 147 salmon rivers, representing three-quarters of the total wild salmon spawning population in Norway. For 109 rivers with adult modern samples and sample sizes of 20 or more, the average level of farmed genetic introgression was 6.4% (median = 2.3%), with a range between 0.0% and 42.2%. Fifty-one of these rivers showed significant farmed genetic introgression when compared with historical reference samples. We observed a highly significant correlation between estimated farmed introgression and average proportion of escaped farmed salmon. We quantify levels of introgression as unweighted averages or weighted by population sizes, to compare geographical regions and to compare levels of introgression in rivers and fjords designated as locations deserving a high level of protection. We found a generally lower level of introgression in National Salmon Rivers and National Salmon Fjords subjected to formal protection by parliament. We conclude that farmed to wild genetic introgression is high in a large proportion of Norwegian salmon rivers, with the highest levels found in the most intensive areas of salmon farming. The extensive genetic introgression documented here poses a serious challenge to the management of farmed and wild Atlantic salmon in Norway and, in all likelihood, in other regions where farmed-salmon escape events occur with regularity

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Introgression from farmed escapees affects the full life cycle of wild Atlantic salmon

Science Advances ◽

10.1126/sciadv.abj3397 ◽

2021 ◽

Vol 7 (52) ◽

Author(s):

Geir H. Bolstad ◽

Sten Karlsson ◽

Ingerid J. Hagen ◽

Peder Fiske ◽

Kurt Urdal ◽

...

Keyword(s):

Life Cycle ◽

Atlantic Salmon ◽

Full Life Cycle ◽

Full Life ◽

Farmed Escapees

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Large-Scale Escapes of Farmed Atlantic Salmon (Salmo salar) into Norwegian Rivers Threaten Natural Populations

Canadian Journal of Fisheries and Aquatic Sciences ◽

10.1139/f91-055 ◽

1991 ◽

Vol 48 (3) ◽

pp. 426-428 ◽

Cited By ~ 95

Author(s):

D. Gausen ◽

V. Moen

Keyword(s):

Atlantic Salmon ◽

Salmo Salar ◽

Large Scale ◽

Natural Populations ◽

Genetic Introgression ◽

Fish Farms ◽

Farmed Salmon ◽

Atlantic Salmon Salmo Salar ◽

Farmed Atlantic Salmon ◽

And Behavior

We present data on Atlantic salmon (Salmo salar) which show that escaped farmed salmon enter Norwegian rivers in great numbers. Escaped farmed salmon comprised a substantial proportion of the mature salmon present on the spawning grounds in autumn. A potential for large-scale genetic introgression thus exists. The sex ratios, length distributions, and times of ascent of wild and farmed salmon differed significantly, reflecting major variations in biology and behavior. High proportions of farmed salmon (> 20%) were found only in rivers having fish farms situated closer than 20 km from the outlet.

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Selection against individuals from genetic introgression of escaped farmed salmon in a natural population of Atlantic salmon

Evolutionary Applications ◽

10.1111/eva.13213 ◽

2021 ◽

Author(s):

Sebastian Wacker ◽

Tonje Aronsen ◽

Sten Karlsson ◽

Ola Ugedal ◽

Ola H. Diserud ◽

...

Keyword(s):

Atlantic Salmon ◽

Natural Population ◽

Genetic Introgression ◽

Farmed Salmon

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Transcriptomic analysis of dead end knockout testis reveals germ cell and gonadal somatic factors in Atlantic salmon

10.21203/rs.2.14111/v1 ◽

2019 ◽

Author(s):

Lene Kleppe ◽

Rolf Brudvik Edvardsen ◽

Tomasz Furmanek ◽

Eva Andersson ◽

Kai Ove Skaftnesmo ◽

...

Keyword(s):

Atlantic Salmon ◽

Germ Cell ◽

Germ Cells ◽

Sertoli Cells ◽

Somatic Cells ◽

The Body ◽

Genetic Introgression ◽

Transcriptome Data ◽

Dead End ◽

Testis Tissue

Abstract Background Sustainability challenges are currently hampering an increase in salmon production. Using sterile salmon can solve problems with precocious puberty and genetic introgression from farmed escapees to wild populations. Recently sterile salmon was produced by knocking out the germ cell-specific dead end (dnd). Several approaches may be applied to inhibit Dnd function, including gene knockout, knockdown or immunization. Since it is challenging to develop a successful treatment against a gene product already existing in the body, alternative targets are being explored. Germ cells are surrounded by, and dependent on, gonadal somatic cells. Targeting genes essential for the survival of gonadal somatic cells may be good alternative targets for sterility treatments. Our aim was to identify and characterize novel germ cell and gonadal somatic factors in Atlantic salmon. Results We have for the first time analysed RNA-sequencing data from germ cell-free (GCF)/dnd knockout and wild type (WT) salmon testis and searched for genes preferentially expressed in either germ cells or gonadal somatic cells. To exclude genes with extra-gonadal expression, our dataset was merged with available multi-tissue transcriptome data. We identified 389 gonad specific genes, of which 194 were preferentially expressed within germ cells, and 11 were confined to gonadal somatic cells. Interestingly, 5 of the 11 gonadal somatic transcripts represented genes encoding secreted TGF-β factors; gsdf, inha, nodal and two bmp6-like genes, all representative vaccine targets. Of these, gsdf and inha had the highest transcript levels. Expression of gsdf and inha was further confirmed to be gonad specific, and their spatial expression was restricted to granulosa and Sertoli cells of the ovary and testis, respectively. Finally, we show that inha expression increases with puberty in both ovary and testis tissue, while gsdf expression does not change or decreases during puberty in ovary and testis tissue, respectively. Conclusions This study contributes with transcriptome data on salmon testis tissue with and without germ cells. We provide a list of novel and known germ cell- and gonad somatic specific transcripts, and show that the expression of two highly active gonadal somatic secreted TGF-β factors, gsdf and inha, are located within granulosa and Sertoli cells.

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Domesticated escapees on the run: the second-generation monitoring programme reports the numbers and proportions of farmed Atlantic salmon in >200 Norwegian rivers annually

ICES Journal of Marine Science ◽

10.1093/icesjms/fsy207 ◽

2019 ◽

Vol 76 (4) ◽

pp. 1151-1161 ◽

Cited By ~ 9

Author(s):

K A Glover ◽

K Urdal ◽

T Næsje ◽

H Skoglund ◽

B Florø-Larsen ◽

...

Keyword(s):

Atlantic Salmon ◽

Second Generation ◽

Fold Increase ◽

Genetic Introgression ◽

Marine Aquaculture ◽

Production Methods ◽

Farmed Salmon ◽

Evolutionary Trajectories ◽

Farmed Atlantic Salmon ◽

Annual Risk

Abstract Norway is the world’s largest producer of farmed Atlantic salmon and is home to ∼400 rivers containing wild salmon populations. Farmed escapees, a reoccurring challenge of all cage-based marine aquaculture, pose a threat to the genetic integrity, productivity, and evolutionary trajectories of wild populations. Escapees have been monitored in Norwegian rivers since 1989, and, a second-generation programme was established in 2014. The new programme includes data from summer angling, autumn angling, broodstock sampling, and snorkelling surveys in >200 rivers, and >25 000 scale samples are analysed annually. In 2014–2017, escapees were observed in two-thirds of rivers surveyed each year, and between 15 and 30 of the rivers had >10% recorded escapees annually. In the period 1989–2017, a reduction in the proportion of escapees in rivers was observed, despite a >6-fold increase in aquaculture production. This reflected improved escape prevention, and possibly changes in production methods that influence post-escape behaviour. On average, populations estimated to experience the greatest genetic introgression from farmed salmon up to 2014 also had the largest proportions of escapees in 2014–2017. Thus, populations already most affected are those at greatest risk of further impacts. These data feed into the annual risk-assessment of Norwegian aquaculture and form the basis for directing mitigation efforts.

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Rescue of germ cells in dnd crispant embryos opens the possibility to produce inherited sterility in Atlantic salmon

Scientific Reports ◽

10.1038/s41598-020-74876-2 ◽

2020 ◽

Vol 10 (1) ◽

Author(s):

Hilal Güralp ◽

Kai O. Skaftnesmo ◽

Erik Kjærner-Semb ◽

Anne Hege Straume ◽

Lene Kleppe ◽

...

Keyword(s):

Atlantic Salmon ◽

Germ Cell ◽

Germ Cells ◽

Large Scale ◽

Environmental Concern ◽

Scale Production ◽

Genetic Introgression ◽

Cell Stage ◽

Novel Approach ◽

Large Scale Production

Abstract Genetic introgression of escaped farmed Atlantic salmon (Salmo salar) into wild populations is a major environmental concern for the salmon aquaculture industry. Using sterile fish in commercial aquaculture operations is, therefore, a sustainable strategy for bio-containment. So far, the only commercially used methodology for producing sterile fish is triploidization. However, triploid fish are less robust. A novel approach in which to achieve sterility is to produce germ cell-free salmon, which can be accomplished by knocking out the dead-end (dnd) gene using CRISPR-Cas9. The lack of germ cells in the resulting dnd crispants, thus, prevents reproduction and inhibits subsequent large-scale production of sterile fish. Here, we report a rescue approach for producing germ cells in Atlantic salmon dnd crispants. To achieve this, we co-injected the wild-type (wt) variant of salmon dnd mRNA together with CRISPR-Cas9 constructs targeting dnd into 1-cell stage embryos. We found that rescued one-year-old fish contained germ cells, type A spermatogonia in males and previtellogenic primary oocytes in females. The method presented here opens a possibility for large-scale production of germ-cell free Atlantic salmon offspring through the genetically sterile broodstock which can pass the sterility trait on the next generation.

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