Research Article: Maternal inheritance of deltamethrin resistance in the salmon louse Lepeophtheirus salmonis (Krøyer) is associated with unique mtDNA haplotypes

Date Published: July 12, 2017

Publisher: Public Library of Science

Author(s): Greta Carmona-Antoñanzas, Michaël Bekaert, Joseph L. Humble, Sally Boyd, William Roy, David I. Bassett, Ross D. Houston, Karim Gharbi, James E. Bron, Armin Sturm, Renfu Shao.

http://doi.org/10.1371/journal.pone.0180625

Abstract

Parasitic infections by the salmon louse, Lepeophtheirus salmonis (Krøyer), cause huge economic damage in salmon farming in the northern hemisphere, with combined treatment costs and production losses in 2014 having been estimated at US$ 350 million for Norway (annual production 1.25 million tonnes). The control of L. salmonis relies significantly on medicinal treatments, supplemented by non-pharmacological approaches. However, efficacy losses have been reported for several delousing agents, including the pyrethroid deltamethrin. The aim of the present study was to analyse the genetic basis of deltamethrin resistance in L. salmonis. Deltamethrin median effective concentrations (EC50) were 0.28 μg L-1 in the drug susceptible L. salmonis strain IoA-00 and 40.1 μg L-1 in the pyrethroid resistant strain IoA-02. IoA-00 and IoA-02 were crossed to produce families spanning one parental and three filial generations (P0, F1-F3). In three families derived from P0 crosses between an IoA-00 sire and an IoA-02 dam, 98.8% of F2 parasites (n = 173) were resistant, i.e. remained unaffected after exposure to 2.0 μg L-1 deltamethrin. F3 parasites from these crosses showed a deltamethrin EC50 of 9.66 μg L-1. In two families of the inverse orientation at P0 (IoA-02 sire x IoA-00 dam), 16.7% of F2 parasites were resistant (n = 84), while the deltamethrin EC50 in F3 animals was 0.26 μg L-1. The results revealed a predominantly maternal inheritance of deltamethrin resistance. The 15,947-nt mitochondrial genome was sequenced and compared among six unrelated L. salmonis strains and parasites sampled from wild salmon in 2010. IoA-02 and three further deltamethrin resistant strains, established from isolates originating from different regions of Scotland, showed almost identical mitochondrial haplotypes. In contrast, the mitochondrial genome was variable among susceptible strains and L. salmonis from wild hosts. Deltamethrin caused toxicity and depletion of whole body ATP levels in IoA-00 but not IoA-02 parasites. The maternal inheritance of deltamethrin resistance and its association with mitochondrial haplotypes suggests that pyrethroid toxicity in L. salmonis may involve molecular targets encoded by mitochondrial genes.

Partial Text

Globally, insecticides play an important role in the control of arthropod disease vectors and crop-infesting pests. However, the development of insecticide resistance reduces the options available for chemical control, which potentially threatens global human health and food security [1–3]. Insecticide resistance in arthropods is based on the emergence and subsequent enrichment of resistance alleles in a population’s gene pool due to selective pressure caused by use of the same or similar acting control agent(s) over several generations [4]. The main molecular mechanisms of insecticide resistance include target site changes disrupting the control agent’s efficacy and the enhanced expression of detoxification mechanisms decreasing internal exposure to the insecticide [5,6].

In reciprocal crosses between a deltamethrin-resistant and a drug-susceptible strain of L. salmonis, maternal inheritance of resistance was observed in families derived from crosses between resistant dams and susceptible sires. In these families, virtually all F2 individuals were resistant, as were 81.2% of F3 parasites. In contrast, in families descended from a susceptible dam and a resistant sire, less than 20% of F2 parasites were resistant while F3 parasites were susceptible.

 

Source:

http://doi.org/10.1371/journal.pone.0180625

 

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