Aquaculture-driven evolution of the salmon louse (Lepeophtheirus salmonis) mtDNA genome

Abstract

Widespread resistance towards pyrethroids, a pesticide that has been extensively used in salmonid aquaculture to control sea lice, is reported in the salmon louse (Lepeophtheirus salmonis). The resistance mechanism has previously been demonstrated to be linked to the mitochondria (mtDNA) genome. The present study aimed to investigate whether widespread pyrethroid usage in salmon aquaculture has caused changes in mitochondrial genetic variation within and among salmon lice in the North Atlantic. This was performed by comparing patterns of genetic variation for two mtDNA genes, ATPase 6 and cytochrome b, and 15 nuclear DNA (nDNA) microsatellites used as controls, between a collection of historical (year 2000 to 2002) and contemporary (year 2014 to 2017) L.salmonis samples collected throughout the North Atlantic. A modest reduction in mtDNA diversity was observed in the period 2000-2017, but no reduction in genetic variation across the 15 microsatellites was observed. An extensive reduction in mtDNA variation was observed in two contemporary samples fixed for one or two haplotypes. In contrast, all historical samples consisted of close to one haplotype per L.salmonis. No population genetic structure was detected among the historical samples for mtDNA nor microsatellites. However, population genetic structure was observed for mtDNA among some of the contemporary samples, which was clearly linked to the drastic change in haplotype frequencies most likely caused by selection for pyrethroid resistance. Collectively, these data support earlier studies concluding that lice are represented by a panmictic population in the North Atlantic, with strong genetic differentiation being observed in small parts of the genome reflecting the transient mosaic pattern of chemical usage and resistance development. Additionally, two previously undetected or historical singleton mtDNA haplotypes increased in frequency in many of the contemporary samples, suggesting a minimum of two origins of pyrethroid resistance for L.salmonis in the North Atlantic. Resistant haplotypes were found in most of the contemporary samples, witnessing the magnitude of dispersal and gene flow in this species. These results demonstrate the need for transatlantic coordination in the use of delousing chemicals to control this parasite.