Compound- and Mixture-Specific Differences in Resistance to Polycyclic Aromatic Hydrocarbons and PCB-126 among<i>Fundulus heteroclitus</i>Subpopulations throughout the Elizabeth River Estuary (Virginia, USA)

Clark, Barry P.; Cooper, Ellen M.; Stapleton, Heather M.; Giulio, Richard T. Di

doi:10.1021/es401604b

Cited by 29 publications

(68 citation statements)

References 60 publications

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“…The high degree of intrapopulation variation in RMO 2 and AS data for least PAH-resistant MC fish may suggest that this is may also be a mixed subpopulation with individuals from more contaminated regions migrating south, a possibility discussed in detail previously. 14 A nongenetic explanation is also plausible, since altered life history strategies at these locations can also lead to reduced AS. Irrespective of the mechanisms, reduced AS in ER fish suggests that aerobic performance and other biological processes (e.g., reproduction and stress responses) might be compromised.…”

Section: Discussionmentioning

confidence: 99%

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Cost of Tolerance: Physiological Consequences of Evolved Resistance to Inhabit a Polluted Environment in Teleost Fish Fundulus heteroclitus

Jayasundara

Fernando

Osterberg

et al. 2017

Environ. Sci. Technol.

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Anthropogenic stressors, including pollutants, are key evolutionary drivers. It is hypothesized that rapid evolution to anthropogenic changes may alter fundamental physiological processes (e.g., energy metabolism), compromising an organism’s capacity to respond to additional stressors. The Elizabeth River (ER) Superfund site represents a “natural-experiment” to explore this hypothesis in several subpopulations of Atlantic killifish that have evolved a gradation of resistance to a ubiquitous pollutant—polycyclic aromatic hydrocarbons (PAH). We examined bioenergetic shifts and associated consequences in PAH-resistant killifish by integrating genomic, physiological, and modeling approaches. Population genomics data revealed that genomic regions encoding bioenergetic processes are under selection in PAH-adapted fish from the most contaminated ER site and ex vivo studies confirmed altered mitochondrial function in these fish. Further analyses extending to differentially PAH-resistant subpopulations showed organismal level bioenergetic shifts in ER fish that are associated with increased cost of living, decreased performance, and altered metabolic response to temperature stress—an indication of reduced thermal plasticity. A movement model predicted a higher energetic cost for PAH-resistant subpopulations when seeking an optimum habitat. Collectively, we demonstrate that pollution adaption and inhabiting contaminated environments may result in physiological shifts leading to compromised organismal capacity to respond to additional stressors.

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Section: Discussionmentioning

confidence: 99%

“…Data are adapted from Clark et al (2013) Table 1 and Figure 2F. 14 *MP data reflects preremediation PAH levels as reported in 2006.…”

Section: Figurementioning

confidence: 99%

Cost of Tolerance: Physiological Consequences of Evolved Resistance to Inhabit a Polluted Environment in Teleost Fish Fundulus heteroclitus

Jayasundara

Fernando

Osterberg

et al. 2017

Environ. Sci. Technol.

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“…However, phenotypes of lower tolerance may not be strongly favored following habitat recovery—or at least not as strongly favored as tolerance phenotypes were following habitat contamination. In fact, one of the contaminated sites in the Elizabeth River (Eppinger and Russell) has undergone significant cleanup and restoration beginning in the mid‐2000s, but fish from this site are still strongly tolerant of DLCs (Clark et al., 2013). Furthermore, because connectivity between polluted habitats and relatively clean habitats is typically limited, migration of fish from historically uncontaminated sites into recently remediated sites could be very slow (Nacci et al., 2008).…”

Section: Ecological Considerationsmentioning

confidence: 99%

When evolution is the solution to pollution: Key principles, and lessons from rapid repeated adaptation of killifish (Fundulus heteroclitus) populations

Whitehead

Clark

Reid

et al. 2017

Evolutionary Applications

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For most species, evolutionary adaptation is not expected to be sufficiently rapid to buffer the effects of human‐mediated environmental changes, including environmental pollution. Here we review how key features of populations, the characteristics of environmental pollution, and the genetic architecture underlying adaptive traits, may interact to shape the likelihood of evolutionary rescue from pollution. Large populations of Atlantic killifish (Fundulus heteroclitus) persist in some of the most contaminated estuaries of the United States, and killifish studies have provided some of the first insights into the types of genomic changes that enable rapid evolutionary rescue from complexly degraded environments. We describe how selection by industrial pollutants and other stressors has acted on multiple populations of killifish and posit that extreme nucleotide diversity uniquely positions this species for successful evolutionary adaptation. Mechanistic studies have identified some of the genetic underpinnings of adaptation to a well‐studied class of toxic pollutants; however, multiple genetic regions under selection in wild populations seem to reflect more complex responses to diverse native stressors and/or compensatory responses to primary adaptation. The discovery of these pollution‐adapted killifish populations suggests that the evolutionary influence of anthropogenic stressors as selective agents occurs widely. Yet adaptation to chemical pollution in terrestrial and aquatic vertebrate wildlife may rarely be a successful “solution to pollution” because potentially adaptive phenotypes may be complex and incur fitness costs, and therefore be unlikely to evolve quickly enough, especially in species with small population sizes.

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“…Several former wood treatment industries contaminated areas of the river with creosote, a complex mixture of chemicals consisting primarily of unsubstituted polycyclic aromatic hydrocarbons (PAHs) and some heterocyclic and phenolic PAHs (Clark et al 2013; Fang et al 2014). Total PAH concentrations at one of the major sites, Atlantic Wood Industries (AW), range from 100-500 μg/g in dry sediment (Mulvey et al 2002; Walker et al 2004).…”

Section: Introductionmentioning

confidence: 99%

Developmental exposure to a complex PAH mixture causes persistent behavioral effects in naive Fundulus heteroclitus (killifish) but not in a population of PAH-adapted killifish

Brown

Bailey

Oliveri

et al. 2016

Neurotoxicology and Teratology

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Acute exposures to some individual polycyclic aromatic hydrocarbons (PAHs) and complex PAH mixtures are known to cause cardiac malformations and edema in the developing fish embryo. However, the heart is not the only organ impacted by developmental PAH exposure. The developing brain is also affected, resulting in lasting behavioral dysfunction. While acute exposures to some PAHs are teratogenically lethal in fish, little is known about the later life consequences of early life, lower dose subteratogenic PAH exposures. We sought to determine and characterize the long-term behavioral consequences of subteratogenic developmental PAH mixture exposure in both naive killifish and PAH-adapted killifish using sediment pore water derived from the Atlantic Wood Industries Superfund Site. Killifish offspring were embryonically treated with two low-level PAH mixture dilutions of Elizabeth River sediment extract (ERSE) (TPAH 5.04 μg/L and 50.4 μg/L) at 24 hours post fertilization. Following exposure, killifish were raised to larval, juvenile, and adult life stages and subjected to a series of behavioral tests including: a locomotor activity test (4 days post-hatch), a sensorimotor response tap/habituation test (3 months post hatch), and a novel tank diving and exploration test (3 months post hatch). Killifish were also monitored for survival at 1, 2, and 5 months over 5-month rearing period. Developmental PAH exposure caused short-term as well as persistent behavioral impairments in naïve killifish. In contrast, the PAH-adapted killifish did not show behavioral alterations following PAH exposure. PAH mixture exposure caused increased mortality in reference killifish over time; yet, the PAH-adapted killifish, while demonstrating long-term rearing mortality, had no significant changes in mortality associated with ERSE exposure. This study demonstrated that early embryonic exposure to PAH-contaminated sediment pore water caused long-term locomotor and behavioral alterations in killifish, and that locomotor alterations could be observed in early larval stages. Additionally, our study highlights the resistance to behavioral alterations caused by low-level PAH mixture exposure in the adapted killifish population. Furthermore, this is the first longitudinal behavioral study to use killifish, an environmentally important estuarine teleost fish, and this testing framework can be used for future contaminant assessment.

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Compound- and Mixture-Specific Differences in Resistance to Polycyclic Aromatic Hydrocarbons and PCB-126 amongFundulus heteroclitusSubpopulations throughout the Elizabeth River Estuary (Virginia, USA)

Cited by 29 publications

References 60 publications

Cost of Tolerance: Physiological Consequences of Evolved Resistance to Inhabit a Polluted Environment in Teleost Fish Fundulus heteroclitus

Cost of Tolerance: Physiological Consequences of Evolved Resistance to Inhabit a Polluted Environment in Teleost Fish Fundulus heteroclitus

When evolution is the solution to pollution: Key principles, and lessons from rapid repeated adaptation of killifish (Fundulus heteroclitus) populations

Developmental exposure to a complex PAH mixture causes persistent behavioral effects in naive Fundulus heteroclitus (killifish) but not in a population of PAH-adapted killifish

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