Page 641 - The Toxicology of Fishes

Toxicity Resistance 621

Costs Associated with Toxicity Resistance

Ecological and evolutionary theory suggests that adaptation to one form of environmental stress may
increase susceptibility to other stressors (Futuyma, 1997). This theory is based on the assumption that
adaptation to a new environment involves alterations in a previous, optimal phenotype that has been
shaped by the various selection pressures of the ancestral environment (Coustau et al., 2000). Alterations
present in the new phenotype should be deleterious to survival in the ancestral environment. Within the
context of adaptation to chemical contaminants, traits that are adaptive for specific chemical contaminants
may present disadvantages under alternate conditions. These disadvantages are often referred to as fitness
costs or fitness trade-offs. There are several possible mechanisms by which development of toxicity
resistance could present disadvantages to adapted individuals (Coustau et al., 2000; Shaw, 1999; Shirley
and Sibly, 1999; Taylor and Feyereisen, 1996): (1) Adaptations that involve alterations in cell targets
(e.g., ion channels) or receptors could disrupt their normal function in the cell and alter higher level
functions in the organism; (2) resistance involving overproduction (induction) of proteins involved in
detoxification or sequestration requires energy and may redirect resources away from growth, reproduc-
tion, or response to other challenges; (3) genes involved in toxicity resistance might be linked to other
cellular processes (i.e., through pleiotrophy) that become unfavorably altered during adaptation to
contaminants; and (4) contaminant-induced selection for tolerance may alter population genetic structure
and reduce genetic diversity in fish populations. Costs associated with alterations in genetic structure
would be dependent on the nature of the alterations themselves.
Despite abundant theory, not a great deal of experimental evidence exists that links toxicity resistance
with reduced fitness in vertebrates. Most progress in this area has been made in studies of insecticide
resistance in insects where pleiotropic effects of insecticide resistance on putative fitness components
have been identified (Raymond et al., 2001). For example, specific alleles involved in pesticide resistance
in mosquitoes have been associated with longer development times and shorter wing spans (Bourguet
et al., 2004). In addition, single-point mutations conferring target-site mutation resistance to DDT in
aphids and houseflies were associated with reduced overwintering survival and decreased response to
alarm pheromones (Foster et al., 2003).

Effects of Contaminants on Specific Fitness Components
Experiments designed to study fitness tradeoffs in fish have involved capturing fish from clean and
contaminated sites and comparing their responses to various stressors under clean laboratory conditions.
Fish that are adapted to contaminated environments often appear less fit in these experiments. Similar
observations in insects and plants have been referred to as between-environment trade-offs, referring to
responses observed after transfer of the study population from the environment to which they have
adapted to another environment (Shirley and Sibley, 1999).
Between-environment trade-offs have been observed in studies with creosote-adapted Atlantic Wood
mummichog. Poor condition (microbial infection, poor growth, emaciation, and increased mortality)
relative to reference fish is routinely observed in Atlantic Wood mummichog maintained in clean estuarine
water (P. Van Veld, pers. commun.). Meyer and Di Giulio (2003) reported similar observations, noting
poor survival of Atlantic Wood F offspring compared to survival of reference F offspring in artificial
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seawater. In addition, Atlantic Wood offspring were more susceptible to mortality associated with low
oxygen (Figure 13.16) and to toxicity associated with photoactivation of PAHs (Meyer and Di Guilio,
2003). The authors concluded that, although the Atlantic Wood mummichogs are adapted to their
contaminated environment, they are maladapted to life in clean environments. The relevance of these
and previously mentioned observations to actual field conditions is uncertain. In the field, the Atlantic
Wood population appears to thrive and do not appear to be experiencing a great deal of mortality due
to low oxygen, phototoxicity, or microbial infection.
Several studies over the past several years have addressed between-environment trade-offs in metal-
tolerant fish populations. Laboratory studies indicate that mummichog collected from the methylmercury-
contaminated environment of Piles Creek in New Jersey appear to be less capable of capturing natural