Transgenerational Effects of Parental Crude Oil Exposure on Gulf Killifish Morphology and Fitness

Abstract

Acute exposure of fish embryos to crude oil adversely affects embryonic development. However, few studies have shown whether exposure of embryos to sublethal concentrations of crude oil has adverse consequences for fish later in life. Even fewer are the number of fish studies assessing the transgenerational effects of chronic oil exposure. The current study determined if a crude oil exposure of adult F0 Gulf killifish (Fundulus grandis) for 36 to 44 days affected the morphology and fitness of adult fish in the F1 and F2 generations despite the progeny being reared in clean water. The F0 fish were used as broodstock to generate four lineages of F1 fish using a full-matrix mating design derived from gametes of clean and oiled parents. Later, the four lineages of F1 fish were used as broodstock to create an F2 generation of the same four lineages. As adults, F1 and F2 fish derived from oiled (grand)parents had altered body shape based on two-dimensional landmark-based geometric morphometrics analyses. Fish from oiled lineages showed changes in body depth, altered spinal curvature, and changes in the angle of projection of the head, which could negatively impact prey capture and swimming. Next, we elucidated the connection between spinal deformity and swim performance in the adult progeny of fish with varying oil exposure histories. We found that both F1 and F2 fish with (grand)paternal oiling displayed significantly higher incidences of spinal deformation than the control lineage. These F1 and F2 fish also performed significantly worse in swimming challenges than non-exposed fish. Lastly, the impacts of parental oil exposure on prey capture abilities, visual responses to virtual prey, and jaw morphology were investigated. We found impaired jaw morphology and striking success in fish derived from a (grand)paternally) exposed lineage across generations. Additionally, feeding impairment observed in this group of paternally oiled killifish was likely due to morphological abnormalities; however, further exploration of potential sensory system perturbations is needed. Based on these findings, we emphasize the need for more long-term, multigenerational studies of the effects of crude oil exposure and the importance of not limiting investigations to early-life endpoints.