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Human-induced evolution caught in action: SNP-array reveals rapid amphi-atlantic spread of pesticide resistance in the salmon ecotoparasite Lepeophtheirus salmonis

BACKGROUND: The salmon louse, Lepeophtheirus salmonis, is an ectoparasite of salmonids that causes huge economic losses in salmon farming, and has also been causatively linked with declines of wild salmonid populations. Lice control on farms is reliant upon a few groups of pesticides that have all s...

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Autores principales: Besnier, Francois, Kent, Matthew, Skern-Mauritzen, Rasmus, Lien, Sigbjørn, Malde, Ketil, Edvardsen, Rolf B, Taylor, Simon, Ljungfeldt, Lina ER, Nilsen, Frank, Glover, Kevin A
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4223847/
https://www.ncbi.nlm.nih.gov/pubmed/25344698
http://dx.doi.org/10.1186/1471-2164-15-937
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author Besnier, Francois
Kent, Matthew
Skern-Mauritzen, Rasmus
Lien, Sigbjørn
Malde, Ketil
Edvardsen, Rolf B
Taylor, Simon
Ljungfeldt, Lina ER
Nilsen, Frank
Glover, Kevin A
author_facet Besnier, Francois
Kent, Matthew
Skern-Mauritzen, Rasmus
Lien, Sigbjørn
Malde, Ketil
Edvardsen, Rolf B
Taylor, Simon
Ljungfeldt, Lina ER
Nilsen, Frank
Glover, Kevin A
author_sort Besnier, Francois
collection PubMed
description BACKGROUND: The salmon louse, Lepeophtheirus salmonis, is an ectoparasite of salmonids that causes huge economic losses in salmon farming, and has also been causatively linked with declines of wild salmonid populations. Lice control on farms is reliant upon a few groups of pesticides that have all shown time-limited efficiency due to resistance development. However, to date, this example of human-induced evolution is poorly documented at the population level due to the lack of molecular tools. As such, important evolutionary and management questions, linked to the development and dispersal of pesticide resistance in this parasite, remain unanswered. Here, we introduce the first Single Nucleotide Polymorphism (SNP) array for the salmon louse, which includes 6000 markers, and present a population genomic scan using this array on 576 lice from twelve farms distributed across the North Atlantic. RESULTS: Our results support the hypothesis of a single panmictic population of lice in the Atlantic, and importantly, revealed very strong selective sweeps on linkage groups 1 and 5. These sweeps included candidate genes potentially connected to pesticide resistance. After genotyping a further 576 lice from 12 full sibling families, a genome-wide association analysis established a highly significant association between the major sweep on linkage group 5 and resistance to emamectin benzoate, the most widely used pesticide in salmonid aquaculture for more than a decade. CONCLUSIONS: The analysis of conserved haplotypes across samples from the Atlantic strongly suggests that emamectin benzoate resistance developed at a single source, and rapidly spread across the Atlantic within the period 1999 when the chemical was first introduced, to 2010 when samples for the present study were obtained. These results provide unique insights into the development and spread of pesticide resistance in the marine environment, and identify a small genomic region strongly linked to emamectin benzoate resistance. Finally, these results have highly significant implications for the way pesticide resistance is considered and managed within the aquaculture industry. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2164-15-937) contains supplementary material, which is available to authorized users.
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spelling pubmed-42238472014-11-08 Human-induced evolution caught in action: SNP-array reveals rapid amphi-atlantic spread of pesticide resistance in the salmon ecotoparasite Lepeophtheirus salmonis Besnier, Francois Kent, Matthew Skern-Mauritzen, Rasmus Lien, Sigbjørn Malde, Ketil Edvardsen, Rolf B Taylor, Simon Ljungfeldt, Lina ER Nilsen, Frank Glover, Kevin A BMC Genomics Research Article BACKGROUND: The salmon louse, Lepeophtheirus salmonis, is an ectoparasite of salmonids that causes huge economic losses in salmon farming, and has also been causatively linked with declines of wild salmonid populations. Lice control on farms is reliant upon a few groups of pesticides that have all shown time-limited efficiency due to resistance development. However, to date, this example of human-induced evolution is poorly documented at the population level due to the lack of molecular tools. As such, important evolutionary and management questions, linked to the development and dispersal of pesticide resistance in this parasite, remain unanswered. Here, we introduce the first Single Nucleotide Polymorphism (SNP) array for the salmon louse, which includes 6000 markers, and present a population genomic scan using this array on 576 lice from twelve farms distributed across the North Atlantic. RESULTS: Our results support the hypothesis of a single panmictic population of lice in the Atlantic, and importantly, revealed very strong selective sweeps on linkage groups 1 and 5. These sweeps included candidate genes potentially connected to pesticide resistance. After genotyping a further 576 lice from 12 full sibling families, a genome-wide association analysis established a highly significant association between the major sweep on linkage group 5 and resistance to emamectin benzoate, the most widely used pesticide in salmonid aquaculture for more than a decade. CONCLUSIONS: The analysis of conserved haplotypes across samples from the Atlantic strongly suggests that emamectin benzoate resistance developed at a single source, and rapidly spread across the Atlantic within the period 1999 when the chemical was first introduced, to 2010 when samples for the present study were obtained. These results provide unique insights into the development and spread of pesticide resistance in the marine environment, and identify a small genomic region strongly linked to emamectin benzoate resistance. Finally, these results have highly significant implications for the way pesticide resistance is considered and managed within the aquaculture industry. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2164-15-937) contains supplementary material, which is available to authorized users. BioMed Central 2014-10-26 /pmc/articles/PMC4223847/ /pubmed/25344698 http://dx.doi.org/10.1186/1471-2164-15-937 Text en © Besnier et al.; licensee BioMed Central Ltd. 2014 This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Besnier, Francois
Kent, Matthew
Skern-Mauritzen, Rasmus
Lien, Sigbjørn
Malde, Ketil
Edvardsen, Rolf B
Taylor, Simon
Ljungfeldt, Lina ER
Nilsen, Frank
Glover, Kevin A
Human-induced evolution caught in action: SNP-array reveals rapid amphi-atlantic spread of pesticide resistance in the salmon ecotoparasite Lepeophtheirus salmonis
title Human-induced evolution caught in action: SNP-array reveals rapid amphi-atlantic spread of pesticide resistance in the salmon ecotoparasite Lepeophtheirus salmonis
title_full Human-induced evolution caught in action: SNP-array reveals rapid amphi-atlantic spread of pesticide resistance in the salmon ecotoparasite Lepeophtheirus salmonis
title_fullStr Human-induced evolution caught in action: SNP-array reveals rapid amphi-atlantic spread of pesticide resistance in the salmon ecotoparasite Lepeophtheirus salmonis
title_full_unstemmed Human-induced evolution caught in action: SNP-array reveals rapid amphi-atlantic spread of pesticide resistance in the salmon ecotoparasite Lepeophtheirus salmonis
title_short Human-induced evolution caught in action: SNP-array reveals rapid amphi-atlantic spread of pesticide resistance in the salmon ecotoparasite Lepeophtheirus salmonis
title_sort human-induced evolution caught in action: snp-array reveals rapid amphi-atlantic spread of pesticide resistance in the salmon ecotoparasite lepeophtheirus salmonis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4223847/
https://www.ncbi.nlm.nih.gov/pubmed/25344698
http://dx.doi.org/10.1186/1471-2164-15-937
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