sea lice, pyrethroids may have an additional target site encoded by the mitochondrial
genome. Maternally inherited, mitochondrially associated pesticide resistance
mechanisms have been infrequently documented, although they do exist [130] and
more work is required to fully understand the role of the mitochondrial encoded
genes in pyrethroid resistance conferral for L. salmonis.
It is important to note that maternal effects may play a role in resistance conferral,
via RNA or protein transferred from the mother to the eggs [126]. This suggestion
also leaves room for the possibility that transgenerational, environmentally induced
epigenetic changes may be contributing to resistance in salmon lice. One recent
study found that non-synonymous base pair substitutions were present in mitochondrial DNA in some pyrethroid-resistant honeybee mites (Varroa destructor) compared with sensitive mites. Further, resistant mites had lower overall levels of DNA
methylation compared with sensitive animals, suggesting that pyrethroid resistance
in these populations may have epigenetic and mitochondrial components [112].
4.2 Resistance in Nontarget Populations
Pyrethroids are not specifically selective for pest insects – they remain toxic to
nontarget arthropods through the same mode of action (as reviewed by Palmquist
et al. [65]). Given that exposure to pyrethroids is the driver selecting for resistance in
a population, it follows that resistance could occur in other arthropods under
selective pressure from these chemicals in their environment. However, pyrethroid
resistance in nontarget populations is a phenomenon that remains more difficult to
quantify than in target populations for several reasons. With the ubiquitous use of
pyrethroid pesticides, it can be difficult to find appropriate control populations
against which to compare those that are suspected to be resistant. It can be difficult
to quantify pyrethroid exposure from terrestrial inputs that move into the aquatic
compartment through agricultural and urban runoff and spray drift. Populations
suspected of being resistant must be screened for phenotypic resistance in a controlled setting, and a genetic marker or other adaptive mechanism of resistance must
also be documented to reasonably conclude that resistance is indeed adaptive rather
than acclimatory or due to maternal effects (Fig. 3). For example, one study induced
a pyrethroid-tolerant phenotype in the cladoceran D. magna by exposing 12 generations to acutely toxic levels of the pyrethroid cyfluthrin and monitoring sensitivity
for an additional 12 generations in the absence of the pyrethroid. D. magna developed a measurable decrease in sensitivity after only four generations (up to 4.8-fold),
which was then lost in 6–10 generations with the absence of exposure [131]. Tolerant
phenotypes were likely conferred via cytochrome P450 activity based on the loss of
resistance with the addition of the P450 inhibitor piperonyl butoxide (PBO). The
authors suggested that the gain and subsequent loss of tolerance were adaptive, but
without more research to determine the mechanistic basis of that tolerance conferral,
the gain and loss of tolerance in D. magna may actually have been caused by
acclimatory and/or maternal effects of cyfluthrin exposure mediated via P450
The Ecological and Evolutionary Implications of Pyrethroid Exposure: A New. . .
123
genome. Maternally inherited, mitochondrially associated pesticide resistance
mechanisms have been infrequently documented, although they do exist [130] and
more work is required to fully understand the role of the mitochondrial encoded
genes in pyrethroid resistance conferral for L. salmonis.
It is important to note that maternal effects may play a role in resistance conferral,
via RNA or protein transferred from the mother to the eggs [126]. This suggestion
also leaves room for the possibility that transgenerational, environmentally induced
epigenetic changes may be contributing to resistance in salmon lice. One recent
study found that non-synonymous base pair substitutions were present in mitochondrial DNA in some pyrethroid-resistant honeybee mites (Varroa destructor) compared with sensitive mites. Further, resistant mites had lower overall levels of DNA
methylation compared with sensitive animals, suggesting that pyrethroid resistance
in these populations may have epigenetic and mitochondrial components [112].
4.2 Resistance in Nontarget Populations
Pyrethroids are not specifically selective for pest insects – they remain toxic to
nontarget arthropods through the same mode of action (as reviewed by Palmquist
et al. [65]). Given that exposure to pyrethroids is the driver selecting for resistance in
a population, it follows that resistance could occur in other arthropods under
selective pressure from these chemicals in their environment. However, pyrethroid
resistance in nontarget populations is a phenomenon that remains more difficult to
quantify than in target populations for several reasons. With the ubiquitous use of
pyrethroid pesticides, it can be difficult to find appropriate control populations
against which to compare those that are suspected to be resistant. It can be difficult
to quantify pyrethroid exposure from terrestrial inputs that move into the aquatic
compartment through agricultural and urban runoff and spray drift. Populations
suspected of being resistant must be screened for phenotypic resistance in a controlled setting, and a genetic marker or other adaptive mechanism of resistance must
also be documented to reasonably conclude that resistance is indeed adaptive rather
than acclimatory or due to maternal effects (Fig. 3). For example, one study induced
a pyrethroid-tolerant phenotype in the cladoceran D. magna by exposing 12 generations to acutely toxic levels of the pyrethroid cyfluthrin and monitoring sensitivity
for an additional 12 generations in the absence of the pyrethroid. D. magna developed a measurable decrease in sensitivity after only four generations (up to 4.8-fold),
which was then lost in 6–10 generations with the absence of exposure [131]. Tolerant
phenotypes were likely conferred via cytochrome P450 activity based on the loss of
resistance with the addition of the P450 inhibitor piperonyl butoxide (PBO). The
authors suggested that the gain and subsequent loss of tolerance were adaptive, but
without more research to determine the mechanistic basis of that tolerance conferral,
the gain and loss of tolerance in D. magna may actually have been caused by
acclimatory and/or maternal effects of cyfluthrin exposure mediated via P450
The Ecological and Evolutionary Implications of Pyrethroid Exposure: A New. . .
123