Aquaculture-driven evolution of the salmon louse mtDNA genome

Resistance towards the antiparasitic pyrethroid, deltamethrin, is reported
in the Atlantic salmon louse (Lepeophtheirus salmonis salmonis), a
persistent ectoparasite of farmed and wild salmonids. The resistance
mechanism is linked to mitochondrial DNA (mtDNA), where genetic markers
for resistance have been identified. Here, we investigated how widespread
pyrethroid use in aquaculture may have influenced mtDNA variation in lice,
and the dispersion of resistant haplotypes across the North Atlantic,
using historical (2000–2002 “pre-resistance”) and contemporary (2014–2017
“post-resistance”) samples. To study this, we sequenced ATPase 6 and
cytochrome b, genotyped two genetic markers for deltamethrin resistance,
and genotyped microsatellites as “neutral” controls of potential
population bottlenecks. Overall, we observed a modest reduction in mtDNA
diversity in the period 2000–2017, but no reduction in microsatellite
variation was observed. The reduction in mtDNA variation was especially
distinct in two of the contemporary samples, fixed for one and two
haplotypes respectively. By contrast, all historical samples consisted of
close to one mtDNA haplotype per individual. No population genetic
structure was detected among the historical samples for mtDNA nor
microsatellites. By contrast, significant population genetic
differentiation was observed for mtDNA among some of the contemporary
samples. However, the observed population genetic structure was tightly
linked with the pattern of deltamethrin resistance, and we therefore
conclude that it primarily reflects the transient mosaic of pyrethroid
usage in time and space. Two historically undetected mtDNA haplotypes
dominated in the contemporary samples, both of which were linked to
deltamethrin resistance, demonstrating primarily two origins of
deltamethrin resistance in the North Atlantic. Collectively, these data
demonstrate that the widespread use of pyrethroids in commercial
aquaculture has substantially altered the patterns of mtDNA diversity in
lice across the North Atlantic, and, that long-distance dispersion of
resistance is rapid due to the high level of genetic connectivity that is
observed in this species.