Accounting for transgenerational effects of toxicant exposure in population models alters the predicted long-term population status

Abstract

Acute environmental stressors such as short-term exposure to pollutants can have lasting effects on organisms, potentially impacting future generations. Parental exposure to toxicants can result in changes to the epigenome (e.g. DNA methylation) that are passed down to subsequent, unexposed generations. However it is difficult to gauge the cumulative population-scale impacts of epigenetic effects from laboratory experiments alone. Here, we developed a size- and age-structured delay-coordinate population model to evaluate the long-term consequences of epigenetic modifications on population sustainability. The model emulated changes in growth, mortality, and fecundity in the F0, F1, and F2 generations observed in experiments in which larval Menidia beryllina were exposed to to environmentally relevant concentrations of bifenthrin, ethinylestradiol (EE2), levonorgestrel, or trenbolone in the parent generation (F0) and reared in clean water up to the F2 generation. Our analysis suggests potentially dramatic population-level effects of repeated, chronic exposures of early life stage fish that are not captured by models not accounting for those effects. Simulated exposures led to substantial declines in population abundance (levonorgestrel and bifenthrin) or near-extinction (EE2 and trenbolone) with the exact trajectory and timeline of population decline dependent on the combination of F0, F1, and F2 effects produced by each compound. Even acute one-time exposures of each compound led to declines and recovery over multiple years due to lagged epigenetic effects. These results demonstrate the potential for environmentally relevant concentrations of commonly used compounds to impact the population dynamics and sustainability of an ecologically relevant species and model organism.

Multigenerational, Indirect Exposure to Pyrethroids Demonstrates Potential Compensatory Response and Reduced Toxicity at Higher Salinity in Estuarine Fish

“…When larval Inland Silversides were exposed to bifenthrin at 10 PSU, fecundity was reduced in the F0 and F1 generations . When population dynamics were modeled in Inland Silversides following early life exposure to bifenthrin at concentrations like those tested here, a steady decline in population was predicted only one year post exposure . However, future studies should test whether population levels stop dropping or rebound if fish are able to adapt.…”

“…11 When population dynamics were modeled in Inland Silversides following early life exposure to bifenthrin at concentrations like those tested here, a steady decline in population was predicted only one year post exposure. 12 However, future studies should test whether population levels stop dropping or rebound if fish are able to adapt. No studies of fish have compared the effects of pyrethroids after multiple generations are exposed concurrently.…”

“…However, they can be highly toxic to nontarget aquatic organisms, including fish . Pyrethroids induce neurotoxicity by causing the continual firing of neurons through the prolonged opening of sodium voltage-gated ion channels, as well as other secondary modes of neurotoxicity such as inhibition of acetylcholinesterase and alteration of calcium and chloride channels. , While pyrethroids are designed to act as neurotoxins at low environmentally relevant concentrations, they have also been found to act as endocrine-disrupting compounds (EDCs), and some pyrethroid metabolites can have stronger estrogenic-like properties than the parent compound. , The endocrine-disrupting effects of pyrethroids lead to altered sex ratios, fecundity, and hatching success, which can have long-term consequences to a population. , Under certain exposure scenarios, this may lead to population decline . Despite this, there are limited studies on the multigenerational effects of pyrethroids in fish .…”

“…10,11 Under certain exposure scenarios, this may lead to population decline. 12 Despite this, there are limited studies on the multigenerational effects of pyrethroids in fish. 13 Multigenerational studies are beneficial since they allow for more population level end points to be measured and for generation-specific impacts to be accounted for, both of which are relevant to pyrethroid exposure, and more so to EDC exposure in general.…”