mechanisms that facilitate phenotypic variation through genotype-environment
interactions. Some environment-genotype interactions may create heritable changes
that can be passed down through germline cells (sperm or egg) referred to as
transgenerational epigenetic inheritance [90]. Epigenetic modifications (also sometimes termed epimutations) involve changes to the DNA structure that are not
reflected in the actual code itself. Epigenetic inheritance mechanisms include methylation, DNA or histone acetylation, self-perpetuating loops, noncoding RNAs, and
structural inheritance [90]. The effects and diversity of epigenetic changes are
complex and still being explored. DNA methylation, for example, in the promoter
region, can decrease gene expression but, in the gene body, may instead cause
increased expression or an increase in splice variants. DNA methylation can also
suppress transposable elements [91]. Epigenetic changes that occur in response to
environmental exposures produce alterations in the gene expression that would
generally qualify them as acclimatory responses, except for the evidence that is
building indicating these changes may sometimes persist transgenerationally in
subsequent unexposed generations [92, 93], suggesting that generations of animals
distantly removed from the environmental conditions that created a given epigenetic
change may be expressing a phenotype based on those changes. In fact, epigenetic
changes such as DNA methylation may provide a direct link between acclimation
and adaptation, since epimutations (methylation at specific locations) may in some
cases increase the likelihood for mutations to occur in a methylated region of DNA
[94]. A growing body of research is investigating whether and how epimutations
may contribute to acclimation and/or adaptation [95].
The emerging field of evolutionary toxicology focuses on the genetic impacts of
pollution on populations. Its relatively recent rise into focus can be attributed largely
to the refinement and expansion of genetic methods that make the study of pollution
effects on population genetics more accessible to researchers [96, 97]. Further,
although epigenetic mechanisms have not explicitly been included in the definition
of evolutionary toxicology, an epigenetic change that persists transgenerationally
would be considered to have an evolutionary significance and as such could fall
within the definition of an adaptive trait [98]. The existence of pollutant-adapted
populations in the wild has implications for human and animal health, evolution,
ecological processes, and risk assessment (see discussion below). However, evolved
pollution responses in wild populations have been historically difficult to characterize, especially in the face of complex mixtures acting on often unknown target sites
[99]. In contrast, as we will show below, pyrethroids’ potency, ubiquitous presence
in the environment, and known mode of action provide an opportunity to more easily
identify and study adaptive responses in populations in comparison to many other
chemical toxicants in the environment.
4.1 Resistance in Target Populations
The most prominent examples of resistance to pyrethroids come from the arthropod
populations these chemicals are designed to eliminate. As with all other classes of
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K. M. Major and S. M. Brander
interactions. Some environment-genotype interactions may create heritable changes
that can be passed down through germline cells (sperm or egg) referred to as
transgenerational epigenetic inheritance [90]. Epigenetic modifications (also sometimes termed epimutations) involve changes to the DNA structure that are not
reflected in the actual code itself. Epigenetic inheritance mechanisms include methylation, DNA or histone acetylation, self-perpetuating loops, noncoding RNAs, and
structural inheritance [90]. The effects and diversity of epigenetic changes are
complex and still being explored. DNA methylation, for example, in the promoter
region, can decrease gene expression but, in the gene body, may instead cause
increased expression or an increase in splice variants. DNA methylation can also
suppress transposable elements [91]. Epigenetic changes that occur in response to
environmental exposures produce alterations in the gene expression that would
generally qualify them as acclimatory responses, except for the evidence that is
building indicating these changes may sometimes persist transgenerationally in
subsequent unexposed generations [92, 93], suggesting that generations of animals
distantly removed from the environmental conditions that created a given epigenetic
change may be expressing a phenotype based on those changes. In fact, epigenetic
changes such as DNA methylation may provide a direct link between acclimation
and adaptation, since epimutations (methylation at specific locations) may in some
cases increase the likelihood for mutations to occur in a methylated region of DNA
[94]. A growing body of research is investigating whether and how epimutations
may contribute to acclimation and/or adaptation [95].
The emerging field of evolutionary toxicology focuses on the genetic impacts of
pollution on populations. Its relatively recent rise into focus can be attributed largely
to the refinement and expansion of genetic methods that make the study of pollution
effects on population genetics more accessible to researchers [96, 97]. Further,
although epigenetic mechanisms have not explicitly been included in the definition
of evolutionary toxicology, an epigenetic change that persists transgenerationally
would be considered to have an evolutionary significance and as such could fall
within the definition of an adaptive trait [98]. The existence of pollutant-adapted
populations in the wild has implications for human and animal health, evolution,
ecological processes, and risk assessment (see discussion below). However, evolved
pollution responses in wild populations have been historically difficult to characterize, especially in the face of complex mixtures acting on often unknown target sites
[99]. In contrast, as we will show below, pyrethroids’ potency, ubiquitous presence
in the environment, and known mode of action provide an opportunity to more easily
identify and study adaptive responses in populations in comparison to many other
chemical toxicants in the environment.
4.1 Resistance in Target Populations
The most prominent examples of resistance to pyrethroids come from the arthropod
populations these chemicals are designed to eliminate. As with all other classes of
118
K. M. Major and S. M. Brander