PBDE Flame Retardant Exposure Causes Neurobehavioral and Transcriptional Effects in First-Generation but Not Second-Generation Offspring Fish

Pollution can have lasting effects beyond the exposure period, potentially impacting multiple generations. Polybrominated diphenyl ether (PBDE) flame retardants are widespread, including in oceans, yet their multigenerational impacts remain poorly understood. We investigated whether BDE-99, a ubiquitous PBDE, induces neurobehavioral and molecular effects across generations in the fish Fundulus heteroclitus. To assess influences of exposure route, we conducted two experiments: in the progenitor exposure, adults were dosed via diet, leading to maternal transfer into F1 eggs; in the direct embryonic exposure, embryos were exposed via water, achieving comparable doses. Both exposures altered larval photomotor responses in F1, but other outcomes differed between exposure route. In the progenitor exposure, maternally exposed F1 juveniles exhibited reduced anxiety-like behavior and altered brain gene expression. In the direct embryonic exposure, F0 fish showed no detectable effects but produced F1 descendants with behavioral changes. This suggests that F1 effects in the progenitor exposure were not driven by chemical transfer alone, but by additional maternal influences. While effects in the progenitor exposure diminished in F2, early behavioral changes were still observed. We conclude that maternal influences shape multigenerational effects of BDE-99 exposure, with exposure route affecting both the nature and persistence of neurobehavioral and molecular outcomes.