Impacts on Atlantic killifish from neurotoxicants: genes, behavior, and population relevant outcomes

Molecular, cellular, and organismal alterations are important descriptors of toxic effects, but our ability to extrapolate and predict ecological risks is limited by the availability of studies that link measurable endpoints to adverse population relevant outcomes such as cohort survival and growth. In this study, we used laboratory gene expression and behavior data from two populations of Atlantic killifish Fundulus heteroclitus (one reference site (SCOKF) and one PCB-contaminated site (NBHKF) to inform individual-based models simulating cohort growth and survival from embryonic exposures to environmentally relevant concentrations of neurotoxicants. Methylmercury exposed SCOKF exhibited brain gene expression changes in the si:ch211-186j3.6, si:dkey-21c1.4, scamp1, and klhl6 genes, which coincided with changes in feeding and swimming behaviors, but our models simulated no growth or survival effects of exposures. PCB126 exposed SCOKF had lower physical activity levels coinciding with a general upregulation in nucleic and cellular brain gene sets (BGS) and down regulation in signaling, nucleic and cellular BGS. The NBHKF, known to be tolerant to PCBs, had altered swimming behaviors that coincided with 98% fewer altered BGS. Our models simulated PCB126 decreased growth in SCOKF and survival in SCOKF and NBHKF. Overall, our study provides a unique demonstration linking molecular and behavioral data to develop quantitative, testable predictions of ecological risk. Overall design: Two populations of Atlantic killifish (KF) were tested, Scorton Creek, Barnstable, MA (SCOKF) and New Bedford Harbor, MA (NBHKF). Embyros were exposed to methylmercury (MeHg) via a parental tuna-based diet resulting in high MeHg KF breeding stock and a salmon-based diet was used to produce low MeHg or reference (control) KF breeding stock [Hg; 186.10 ± 23.30 ng tHg/g dw KF, standard deviation (SD), n=5, sampled April 27, 2017). The low MeHg KF breeding stock received a daily estimated dose of ~ 300 ng tHg/g dw KF/day through their salmon-based diet resulting in a lower MeHg body concentration [162.46 ± 20.21 ng tHg/g dw KF (SD, n=8)]. Subsamples of the embryos from SCOKF Low MeHg diet and NBHKF Low MeHg diet KF were exposed directly during development, 1 to 7 days post fertilization, with 40 or 400 ng/L PCB126.