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

Abstract

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.

Genome-wide scan reveals signatures of selection related to pollution adaptation in non-model estuarine Atlantic killifish (Fundulus heteroclitus)

“…Furthermore, certain CYB5 variants in humans result in heritable methemoglobinemia type IV (Hegesh et al, 1986), a condition that causes a buildup of methemoglobin, and a subsequent reduction in oxygen carrying capacity. Similar outcomes of CYB5 gene changes in AW killifish could contribute to the physiological costs of the Elizabeth River adaptations reported in (Jayasundara et al, 2017).…”

Combined effects of elevated temperature and Deepwater Horizon oil exposure on the cardiac performance of larval mahi-mahi, Coryphaena hippurus

“…As previously described, strong upregulation of genes not associated with the AhR pathway were observed, but it has also been found that the detoxification mechanisms were significantly upregulated in exposed larvae [ 23 , 68 ]. Strong induction of AhR detoxifying systems are not only energetically costly for organisms but also might be responsible for cardiac failure in larvae after oil exposure [ 30 , 69 – 71 ]. Environmental temperature also influences the level of various xenobiotic metabolizing enzyme activities in fish exposed to crude oil [ 58 , 59 ].…”

Evolutionary responses of marine organisms to urbanized seascapes

“…However, consecutive stressors can, in some cases, have larger impacts on individuals and populations than simultaneous stressors, as in the case of acidified conditions and salinity in crab larvae (Miller et al, 2014) and consecutive warmer air and water temperatures in sea stars (Pincebourde, Sanford, Casas, & Helmuth, 2012), if exposure to the first stressor causes physiological changes that leave an organism vulnerable to a second stressor (e.g., Todgham & Stillman, 2013). Jayasundara et al (2017) showed that killifish adapted to polluted waterways demonstrated altered metabolic and physiological responses to other stressors such as temperature, indicating that adaptation to pollution may compromise the ability of this population to acclimate to other stressors. In addition, each stressor may be inconsistent and may fluctuate over time.…”

“…Jayasundara et al. (2017) showed that killifish adapted to polluted waterways demonstrated altered metabolic and physiological responses to other stressors such as temperature, indicating that adaptation to pollution may compromise the ability of this population to acclimate to other stressors. In addition, each stressor may be inconsistent and may fluctuate over time.…”