Losing the 'arms race': Multiresistant salmon lice are dispersed throughout the North Atlantic Ocean

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.publishedVersio

Effects of the geoindex or the kernel density of treatments (KD) on the proportion of mutated genotypes.

<p>GAM-plots showing the non-linear relative effects of the geoindex (left panel) or kernel density of treatments (KD) on the proportion of mutated genotypes (RR or RS) in farm sampled salmon lice. The two plots represent univariate fitting of the proportion model. The relationship between farm geoindexes and their north coordinate is also shown (right panel).</p

<i>Phe362Tyr</i> in AChE: A Major Factor Responsible for Azamethiphos Resistance in <i>Lepeophtheirus salmonis</i> in Norway

<div><p>Organophosphates (OP) are one of the major treatments used against the salmon louse (<i>Lepeophtherius salmonis</i>) in Norwegian salmonid aquaculture. The use of OP since the late 1970s has resulted in widespread resistant parasites. Recently, we reported a single mutation (<i>Phe362Tyr</i>) in acetylcholinesterase (AChE) as the major mechanism behind resistance in salmon louse towards OP. The present study was carried out to validate this mechanism at the field level. A total of 6658 salmon louse samples were enrolled from 56 different fish farms across the Norwegian coast, from Vest Agder in the south to Finnmark in the north. All the samples were genotyped using a TaqMan probe assay for the <i>Phe362Tyr</i> mutation. A strong association was observed between areas with frequent use of the OP (azamethiphos) and the <i>Phe362Tyr</i> mutation. This was confirmed at 15 sites where results from independently conducted bioassays and genotyping of parasites correlated well. Furthermore, genotyping of surviving and moribund parasites from six bioassay experiments demonstrated a highly significant negative correlation between the frequency of resistance alleles and the probability of dying when exposed to azamethiphos in a bioassay. Based on these observations, we could strongly conclude that the <i>Phe362Tyr</i> mutation is a major factor responsible for OP resistance in salmon louse on Norwegian fish farms.</p></div

Relative quantities of the kernel density of treatments along with the geoindex line.

<p>Maps showing relative quantities of the kernel density of treatments along with the geoindex line (left panel), and the proportion of the SS, RS and RR genotypes (right panel, note that locations of farms are displaced in areas with clusters of farms to avoid overlapping symbols).</p

A summary of outcomes of salmon louse viability in bioassay tests at different concentrations of azamethiphos.

<p>The average % immobilized and alive parasites in the 15 assays, and their standard deviation, are given. The total number of parasites are also given.</p

General linear model (GLM) for the binomial outcome of salmon louse exposure to azamethiphos in bioassay tests tests (Coeff refers to regression coefficient and SEM to standard error of mean).

<p>General linear model (GLM) for the binomial outcome of salmon louse exposure to azamethiphos in bioassay tests tests (Coeff refers to regression coefficient and SEM to standard error of mean).</p

The number of farms reporting the use of azamethiphos, the total number of treatment reports and the accumulated number of treatments, for the years 2012–2014.

<p>The number of farms reporting the use of azamethiphos, the total number of treatment reports and the accumulated number of treatments, for the years 2012–2014.</p

Final mixed logistic model for lice-level mortality in bioassay tests (Coeff refers to regression coefficient and SEM to standard error of mean).

<p>AIC in the full model was 17889.</p

The mechanism (Phe362Tyr mutation) behind resistance in Lepeophtheirus salmonis pre-dates organophosphate use in salmon farming

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