Resistance to polycyclic aromatic hydrocarbon toxicity and associated bioenergetic consequences in a population of Fundulus heteroclitus

Abstract

Several locations in the Elizabeth River, VA, USA are highly contaminated with polycyclic aromatic hydrocarbons (PAHs), due to the release of creosote mixtures from wood treatment facilities. Interestingly, some populations of Atlantic killifish (Fundulus heteroclitus) inhabiting the Elizabeth River (ER) are resistant to PAH-induced teratogenesis. However, evolutionary resistance to PAHs due to chronic PAH exposure is associated with reduced fitness and increased susceptibility to other environmental stressors in at least one PAH-resistant ER killifish population. More specifically, wild-caught and first generation PAH-resistant juvenile killifish have altered metabolic demands when compared to non-resistant fish. Herein, we investigated this association further by examining a previously under-studied population captured from the creosote-contaminated site Republic Creosoting (Rep). We assessed PAH toxicity and effects on energy metabolism in Rep killifish in comparison with killifish from the reference site Kings Creek (KC). Following exposures to simple and complex PAH mixtures, Rep killifish exhibited several phenotypes associated with PAH resistance including decreased incidences of developmental cardiovascular deformities and recalcitrant cytochrome P450 1A (CYP1A) activity. We evaluated bioenergetics in killifish embryos throughout development and found elevated basal oxygen consumption rates in Rep embryos relative to KC embryos. Furthermore, juvenile F1 Rep fish had significantly lower maximal metabolic rates and aerobic scopes than KC juveniles. These results suggest that populations of killifish that have adapted or evolved to withstand the toxicity associated with PAHs consequently have altered energetic metabolism or demands. Such consequences could result in an enhanced vulnerability to other environmental and anthropogenic stressors in PAH-resistant killifish.

Altered lipid homeostasis in a PCB-resistant Atlantic killifish (Fundulus heteroclitus) population from New Bedford Harbor, MA, U.S.A.

“…Conventional scientific theory of evolution and adaptation to environmental pollutants suggests that fitness costs ensue because the original, and presumably optimal, phenotype has been altered (Coustau, Chevillon, & ffrench-Constant, 2000; reviewed in Whitehead et al, 2017). A few examples that have been identified in some pollution-adapted killifish populations (but not including NBH) include altered bioenergetics (Jayasundara et al, 2017;Lindberg et al, 2017) and increased susceptibility to hypoxia (Meyer and Di Giulio, 2003), oxidative stress (Harbeitner et al, 2013), and infectious disease (Frederick et al, 2007).…”

Liver biomarkers response of the neotropical fish Aequidens metae to environmental stressors associated with the oil industry

“…This effect could be linked to the presence of PAHs and other pollutants that are also inducers of this activity. Increased EROD activity has been reported in fish exposed to a wide range of pollutants, such as PAHs, polychlorinated biphenyls, and tetrachlorodibenzo-p-dioxin ( Basu et al., 2004 ; Gagnon and Rawson, 2016 ; Lindberg et al., 2017 ). In a series of in vitro studies, an increase of EROD activity has been described and characterized in a rainbow trout liver derived cell line exposed to the water accommodated fraction (WAF) of oil samples collected from an oil spill (Prestige oil spill, in the North-West of Spain) ( Navas et al., 2006 ).…”

Evolutionary Toxicology—An Informational Tool for Chemical Regulation?

“…; Lindberg et al. ). It has been further argued that the genetic diversity lost through adaptation to pollution can “erode evolutionary potential,” making species less able to confront novel environmental challenges (Laroche et al.…”