Induced pesticide tolerance results from detoxification pathway priming

Oziolor, Elias M.; Howard, W. Brian; Lavado, Ramón; Matson, Cole W.

doi:10.1016/j.envpol.2017.02.046

Cited by 7 publications

(7 citation statements)

References 41 publications

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“…The induction of increased tolerance following sublethal exposure to carbaryl may buffer sensitive aquatic species from the negative effects associated with anthropogenic contaminants . Increased tolerance to pesticides may occur through a variety of processes including the increased metabolism of pesticides following upregulation of detoxifying enzymes, targeted compounds, and pathways, or through target-site mutations that inhibit proper pesticide binding. ,,, For example, Oziolor et al reported increased tolerance to carbaryl in Gulf killifish ( Fundulus grandis ) previously exposed to sublethal carbaryl concentrations following the activation of the aryl hydrocarbon receptor pathway and increase in cytochrome P450 1A activity. The combination of detoxification pathways and genes , with increased production of acetylcholine esterase following sublethal pesticide exposure might buffer amphibians from agrochemical contamination.…”

Section: Discussionmentioning

confidence: 99%

Inducible Tolerance to Agrochemicals Was Paved by Evolutionary Responses to Predators

Jones

Hintz

Schuler

et al. 2017

Environ. Sci. Technol.

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Recent research has reported increased tolerance to agrochemicals in target and nontarget organisms following acute physiological changes induced through phenotypic plasticity. Moreover, the most inducible populations are those from more pristine locations, far from agrochemical use. We asked why do populations with no known history of pesticide exposure have the ability to induce adaptive responses to novel agrochemicals? We hypothesized that increased pesticide tolerance results from a generalized stressor response in organisms, and would be induced following sublethal exposure to natural and anthropogenic stressors. We exposed larval wood frogs (Lithobates sylvaticus) to one of seven natural or anthropogenic stressors (predator cue (Anax spp.), 0.5 or 1.0 mg carbaryl/L, road salt (200 or 1000 mg Cl/L), ethanol-vehicle control, or no-stressor control) and subsequently tested their tolerance to a lethal carbaryl concentration using time-to-death assays. We observed induced carbaryl tolerance in tadpoles exposed to 0.5 mg/L carbaryl and also in tadpoles exposed to predator cues. Our results suggest that the ability to induce pesticide tolerance likely arose through evolved antipredator responses. Given that antipredator responses are widespread among species, many animals might possess inducible pesticide tolerance, buffering them from agrochemical exposure.

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Section: Discussionmentioning

confidence: 99%

Inducible Tolerance to Agrochemicals Was Paved by Evolutionary Responses to Predators

Jones

Hintz

Schuler

et al. 2017

Environ. Sci. Technol.

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“…These results highlight the complex interactions between evolved responses that enable amphibian larvae to respond to numerous environmental stressors (Laurila et al 2002, Benard 2004, Hossie et al 2017). Future research examining the genetic and developmental basis for such responses (Oziolor et al 2017 a , b ) will enable researchers to identify how evolved responses to human stressors might influence a suite of related traits.…”

Section: Discussionmentioning

confidence: 99%

Predator‐ and competitor‐induced responses in amphibian populations that evolved different levels of pesticide tolerance

Jones

Hua

Mattes

et al. 2021

Ecological Applications

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Exposure to agrochemicals can drive rapid phenotypic and genetic changes in exposed populations. For instance, amphibian populations living far from agriculture (a proxy for agrochemical exposure) exhibit low pesticide tolerance, but they can be induced to possess high tolerance following a sublethal pesticide exposure. In contrast, amphibian populations close to agriculture exhibit high, constitutive tolerance to pesticides. A recent study has demonstrated that induced pesticide tolerance appears to have arisen from plastic responses to predator cues. As a result, we might expect that selection for constitutive pesticide tolerance in populations near agriculture (i.e., genetic assimilation) will lead to the evolution of constitutive responses to natural stressors. Using 15 wood frog (Rana sylvatica) populations from across an agricultural gradient, we conducted an outdoor mesocosm experiment to examine morphological (mass, body length, and tail depth) and behavioral responses (number of tadpoles observed and overall activity) of tadpoles exposed to three stressor environments (no-stressor, competitors, or predator cues). We discovered widespread differences in tadpole traits among populations and stressor environments, but no population-by-environment interaction. Subsequent linear models revealed that population distance to agriculture (DTA) was occasionally correlated with tadpole traits in a given environment and with magnitudes of plasticity, but none of the correlations were significant after Bonferroni adjustment. The magnitudes of predator and competitor plasticity were never correlated with the magnitude of pesticide-induced plasticity that we documented in a companion study. These results suggest that while predator-induced plasticity appears to have laid the foundation for the evolution of pesticide-induced plasticity and its subsequent genetic assimilation, inspection of population-level differences in plastic responses show that the evolution of pesticide-induced plasticity has not had a reciprocal effect on the evolved plastic responses to natural stressors.

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“…While the mechanism allowing D. pulex to induce carbaryl tolerance is not yet known, in wood frogs, individuals that induced tolerance had higher levels of AChE (Hua et al, ). In killifish, individuals with inducible tolerance had increased activity of cytochrome P450 1A (CYP1A), which increased the ability to metabolize carbaryl (Oziolor et al, ). Therefore, early exposure to sublethal carbaryl may have induced D. pulex to upregulate and accumulate AChE protecting them from later exposures (Hua et al, ).…”

Section: Discussionmentioning

confidence: 99%

“…Therefore, early exposure to sublethal carbaryl may have induced D. pulex to upregulate and accumulate AChE protecting them from later exposures (Hua et al, ). Alternatively, D. pulex may have induced increased cytochrome P450‐ mediated xenobiotic metabolism activity, increasing their ability to metabolize carbaryl (Oziolor et al, ). As human activities continue to encroach upon natural systems, considering the role of plasticity in allowing wild populations to respond to rapidly changing conditions and identifying the mechanisms driving these rapid plastic responses has broad conservation implications.…”

Section: Discussionmentioning

confidence: 99%

“…The ability to rapidly induce tolerance may play a significant role in the persistence of aquatic organisms exposed to pesticides as many taxa are confined to the boundaries of the aquatic environment and cannot disperse to avoid exposure to contaminants (Moe et al, ). However, to date, the phenomenon of inducible tolerance to pesticides is known to occur only in 4 species: wood frogs, gray tree frogs, gulf killifish, and yellow‐fever mosquitos (Hua et al, ; Jones & Relyea, ; Oziolor, Howard, Lavado, & Matson, ; Poupardin et al, ). Given the ubiquitous nature of pesticide contamination in freshwater ecosystems, considering both constitutive and inducible mechanisms for tolerance is critical to developing a better understanding of whether and how natural communities will respond to contaminants (Stone et al, ).…”

Section: Introductionmentioning

confidence: 99%

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Inducible pesticide tolerance in Daphnia pulex influenced by resource availability

Wuerthner

Jaeger

Garramone

et al. 2019

Ecology and Evolution

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Pesticides are a ubiquitous contaminant in aquatic ecosystems. Despite the relative sensitivity of aquatic species to pesticides, growing evidence suggests that populations can respond to pesticides by evolving higher baseline tolerance or inducing a higher tolerance via phenotypic plasticity. While both mechanisms can allow organisms to persist when faced with pesticides, resource allocation theory suggests that tolerance may be related to resource acquisition by the organism. Using Daphnia pulex, we investigated how algal resource availability influenced the baseline and inducible tolerance of D. pulex to a carbamate insecticide, carbaryl. Individuals reared in high resource environments had a higher baseline carbaryl tolerance compared to those reared in low resource environments. However, D. pulex from low resource treatments exposed to sublethal concentrations of carbaryl early in development induced increased tolerance to a lethal concentration of carbaryl later in life. Only individuals reared in the low resource environment induced carbaryl tolerance. Collectively, this highlights the importance of considering resource availability in our understanding of pesticide tolerance.

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Induced pesticide tolerance results from detoxification pathway priming

Cited by 7 publications

References 41 publications

Inducible Tolerance to Agrochemicals Was Paved by Evolutionary Responses to Predators

Inducible Tolerance to Agrochemicals Was Paved by Evolutionary Responses to Predators

Predator‐ and competitor‐induced responses in amphibian populations that evolved different levels of pesticide tolerance

Inducible pesticide tolerance in Daphnia pulex influenced by resource availability

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