Dietary pollutants induce oxidative stress, altering maternal antioxidant provisioning and reproductive output in the temperate sea urchin Evechinus chloroticus

Abstract

Evidence is growing to suggest that the capacity to withstand oxidative stress may play an important role in shaping life-history trade-offs, although little is known on the relationship in broadcast spawning marine invertebrates. In this group, variation in gamete quantity and quality are important drivers of offspring survival and successful recruitment. Therefore the provisioning of eggs with antioxidants may be an important driver of life history strategies because they play a critical role in preventing damage from reactive oxygen species to macromolecules. In this study, a suite of oxidative stress biomarkers was measured in the gonads and eggs of the sea urchin Evechinus chloroticus exposed to polycyclic aromatic hydrocarbons (PAHs). Links between oxidative stress markers and core components of fitness including fecundity, gamete quality and maternal transfer of antioxidants were assessed. Experimental induction of oxidative stress was achieved via exposure to a mix of four PAHs over a 21-day period. In PAH exposed individuals, we observed a significant upregulation of the antioxidant defence and detoxification enzymes SOD, CAT, GR, GPx and GST, as well as a greater pool of the non-enzymatic antioxidant glutathione in gonad tissue and eggs. In contrast, glutathione redox status was not affected by PAH exposure, with the percentage of reduced glutathione remaining at approximately 80% in both gonad tissue and released eggs. PAH-exposed adults experienced greater than three- and five-fold increases in oxidative protein and lipid damage, respectively, in gonad tissue. In contrast, eggs maintained low levels of damage, not differing from baseline levels found in eggs released from PAH-naïve mothers. PAH exposure also resulted in a 2-fold reduction in fecundity of reproductively mature females but no significant alteration to egg diameter. Although PAH-exposed females released fewer eggs, successful fertilisation of those eggs was slightly enhanced with average rates ranging from 90-99% in comparison to 76-90% in control eggs. Early-stage offspring reflected maternal antioxidant status with populations derived from PAH-exposed mothers demonstrating significantly higher antioxidant levels than those derived from PAH-naïve mothers. This maternally inherited protection enhanced the capacity of embryos to minimise oxidative damage to lipids and proteins during early development but, despite this, did not reduce the proportion of morphological abnormalities in the population. Overall, these findings indicate that when faced with short-term contaminant stress E. chloroticus has the capacity to trade high reproductive output during a spawning event for a greater antioxidant investment in eggs. However, this production of potentially more resilient offspring did not translate to a fitness gain, at least for the early larval stages in the present experimental conditions.

Keywords: Antioxidant; Evechinus chloroticus; Life-history; Oxidative stress; Pollutants.