Abstract
Ongoing sea-ice decline and expanding industrial activity in the Arctic increase the risk of crude oil exposure in ecosystems where fish reproduction is tightly synchronized with seasonal environmental cues. We conducted in vivo experiments to examine how exposure to the water-soluble fraction (WSF) of crude oil during late vitellogenesis affects reproductive development, spawning phenology, and intergenerational outcomes in polar cod (Boreogadus saida) and Atlantic cod (Gadus morhua). Repeated experiments in these gadids consistently demonstrated advancement of spawning following exposure at advanced vitellogenesis, indicating reproducible effects. In polar cod, spawning was significantly and dose-dependently advanced without detectable effects on gonadal structure, gamete quality, fertilization success, or sperm performance. However, subtle alterations in plasma sex steroids and expression of genes involved in ovarian steroidogenesis suggested endocrine modulation of pathways regulating final oocyte maturation. Sustained PAH metabolite levels indicated prolonged internal exposure and possible complex mixture effects. To assess intergenerational consequences, offspring of exposed Atlantic cod were produced via controlled in vitro crosses. Maternal exposure resulted in a marked downregulation of genes involved in early development, and a complete embryo mortality before hatching. Paternal exposure caused minimal transcriptomic effects, but reduced early larval survival, suggesting delayed or epigenetic impacts. Together, these findings show that crude oil exposure affects sensitive life stages in adults and can compromise next-generation viability. Even modest phenological shifts may influence recruitment success, highlighting the need to integrate multigenerational endpoints into population-level risk assessments for Arctic fish.