Abstract
Antiparasitic drugs such as emamectin benzoate (EMB) are relied upon to reduce the parasite load, particularly of the sea louse Lepeophtheirus salmonis, on farmed salmon. The decline in EMB treatment efficacy for this purpose is an important issue for salmon producers around the world, and particularly for those in the Atlantic Ocean where widespread EMB tolerance in sea lice is recognized as a significant problem. Salmon farms in the Northeast Pacific Ocean have not historically experienced the same issues with treatment efficacy, possibly due to the relatively large population of endemic salmonid hosts that serve to both redistribute surviving lice and dilute populations potentially under selection by introducing naïve lice to farms. Frequent migration of lice among farmed and wild hosts should limit the effect of farm-specific selection pressures on changes to the overall allele frequencies of sea lice in the Pacific Ocean. A previous study using microsatellites examined L. salmonis oncorhynchi from 10 Pacific locations from wild and farmed hosts and found no population structure. Recently however, a farm population of sea lice was detected where EMB bioassay exposure tolerance was abnormally elevated. In response, we have developed a Pacific louse draft genome that complements the previously-released Atlantic louse sequence. These genomes were combined with whole-genome re-sequencing data to design a highly sensitive 201,279 marker SNP array applicable for both subspecies (90,827 validated Pacific loci; 153,569 validated Atlantic loci). Notably, kmer spectrum analysis of the re-sequenced samples indicated that Pacific lice exhibit a large within-individual heterozygosity rate (average of 1 in every 72 bases) that is markedly higher than that of Atlantic individuals (1 in every 173 bases). The SNP chip was used to produce a high-density map for Atlantic sea louse linkage group 5 that was previously shown to be associated with EMB tolerance in Atlantic lice. Additionally, 478 Pacific louse samples from farmed and wild hosts obtained between 2005 and 2014 were also genotyped on the array. Clustering analysis allowed us to detect the apparent emergence of an otherwise rare genotype at a high frequency among the lice collected from two farms in 2013 that had reported elevated EMB tolerance. This genotype was not observed in louse samples collected from the same farm in 2010, nor in any lice sampled from other locations prior to 2013. However, this genotype was detected at low frequencies in louse samples from farms in two locations reporting elevated EMB tolerance in 2014. These results suggest that a rare genotype present in Pacific lice may be locally expanded in farms after EMB treatment. Supporting this hypothesis, 437 SNPs associated with this genotype were found to be in a region of linkage group 5 that overlaps the region associated with EMB resistance in Atlantic lice. Finally, five of the top diagnostic SNPs within this region were used to screen lice that had been subjected to an EMB survival assay, revealing a significant association between these SNPs and EMB treatment outcome. To our knowledge this work is the first report to identify a genetic link to altered EMB efficacy in L. salmonis in the Pacific Ocean.
Highlights
The salmon aquaculture industry is a major global economic contributor, with a production of 3.2 million tonnes in 2013 worth nearly US$18 billion (Food and Agriculture Organization of the United Nations and Fisheries and Aquaculture Department, 2014)
By mapping the additional 37 libraries (NCBI Bioproject: PRJNA447894) to the Atlantic and Pacific reference sequences, the single nucleotide polymorphism (SNP) necessary for SNP chip construction were identified: 5198 SNPs were included from previous studies (Group 1), 4959 SNPs were emamectin benzoate (EMB) response-linked (Group 2), 62,404 SNPs were present in putative transcripts from both Atlantic and Pacific lice (Group 3), 96,082 were from non-coding regions in Atlantic sea lice (Group 4) and 32,636 SNPs were rare Atlantic SNPs (Group 5)
The removal of the sex-linked markers, which interfered with our ability to interpret population-level differences, allowed us to directly address the following question: do patterns of non-neutral genomic differentiation exist among groups of Pacific sea lice? As shown in Fig. 4, we found a narrow region of linkage group 5 containing a multilocus SNP genotype that could be used to sort lice into two distinct clusters (Fig. 1)
Summary
The salmon aquaculture industry is a major global economic contributor, with a production of 3.2 million tonnes in 2013 worth nearly US$18 billion (Food and Agriculture Organization of the United Nations and Fisheries and Aquaculture Department, 2014). One of the most publicized concerns with aquaculture farms in British Columbia in the last decade surround infestations of the parasitic copepod Lepeophtheirus salmonis, commonly referred to as salmon or sea lice. Sea louse infestations are a major concern to the global salmon farming industry, with the most recent estimates of the cost to industry between 4 and 10% of the global value of salmon production in 2008 (Mustafa et al, 2001). In British Columbia in particular a major public focus has been on the role salmon farming may play in increasing the parasite load on vulnerable wild salmon, given the common placement of farms in sheltered inlets which lay along the migratory path of juvenile wild salmon The parasite load on farms is managed in part to reduce the risk of transfer of lice from farmed to wild salmon. After industry requests for access to an EMB alternative, partially driven by observations of reduced EMB efficacy in some farms, permits were granted in BC for limited regional use of hydrogen peroxide baths in 2014 (http:// www.marineharvest.ca/about/news-and-media/container/april-102014/)
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