The parasitic salmon louse, and its resistance to chemical delousing agents, represents one of the largest challenges to the salmon aquaculture industry. We genotyped lice sampled from wild salmon and sea trout throughout Norway with the recently identified Phe362Tyr mutation that conveys resistance to organophosphates. These results were compared to data from lice sampled on farmed salmon in the same regions. The resistant (R) allele was observed in salmon lice from wild salmon and sea trout throughout Norway, although its frequency was highest in farming-intense regions. In most regions, the frequency of the R allele was higher in lice collected from wild sea trout than wild Atlantic salmon, and in all regions, the frequency of the R allele was similar in lice collected from wild sea trout and farmed Atlantic salmon. The R allele is only selected for in fish-farms where organophosphates are used for delousing. Therefore, our results suggest extensive exchange of lice between farmed and wild hosts, and indicate that in farming-dense regions in Norway, aquaculture represents a major driver of salmon louse population structure. Finally, these data suggest that the wild hosts within the regions studied will not delay the spread of resistance when organophosphates are used.

The salmon louse is an ectoparasitic copepod of salmonids in the marine environment, and represents a global challenge to salmon aquaculture. A major issue is the reliance of the industry on a limited number of chemicals to delouse salmonids on farms, and the high levels of resistance that lice have developed to all of these agents. However, for most of these chemicals, resistance and dispersal mechanisms are unknown. We recently demonstrated that the Phe362Tyr mutation is the primary cause of organophosphate resistance in lice collected on Norwegian farms. In the present study, we genotyped >2000 lice collected throughout the entire North Atlantic in the period 1998–2016, using Phe362Tyr and nine tightly linked SNPs. Our results showed that the Phe362Tyr mutation is strongly linked to lice survival following chemical treatment on farms located throughout the North Atlantic, demonstrating for the first time, that this mutation represents the primary mechanism for organophosphate resistance in salmon lice across the North Atlantic. Additionally, we observed multiple and diverse high frequency haplotypes linked with the allele conveying resistance to organophosphate. We, therefore, conclude that Phe362Tyr is not a de novo mutation, but probably existed in salmon lice before the introduction of organophosphates in commercial aquaculture.

Nothing lasts forever, including the effect of chemicals aimed to control pests in food production. As old pesticides have been compromised by emerging resistance, new ones have been introduced and turned the odds back in our favour. With time, however, some pests have developed multi-pesticide resistance, challenging our ability to control them. In salmonid aquaculture, the ectoparasitic salmon louse has developed resistance to most of the available delousing compounds. The discovery of genetic markers associated with resistance to organophosphates and pyrethroids made it possible for us to investigate simultaneous resistance to both compounds in approximately 2000 samples of salmon lice from throughout the North Atlantic in the years 2000–2016. We observed widespread and increasing multiresistance on the European side of the Atlantic, particularly in areas with intensive aquaculture. Multiresistant lice were also found on wild Atlantic salmon and sea trout, and also on farmed salmonid hosts in areas where delousing chemicals have not been used. In areas with intensive aquaculture, there are almost no lice left that are sensitive to both compounds. These results demonstrate the speed to which this parasite can develop widespread multiresistance, illustrating why the aquaculture industry has repeatedly lost the arms race with this highly problematic parasite.