Short-term anoxic conditioning hormesis boosts antioxidant defenses, lowers oxidative damage following irradiation and enhances male sexual performance in the Caribbean fruit fly, Anastrepha suspensa

Abstract

SUMMARY Most organisms are repeatedly exposed to oxidative stress from multiple sources throughout their lifetimes, potentially affecting all aspects of organismal performance. Here we test whether exposure to a conditioning bout of anoxia early in adulthood induces a hormetic response that confers resistance to oxidative stress and enhances male sexual performance later in life in the Caribbean fruit fly, Anastrepha suspensa. Anoxic conditioning of adults prior to emergence led to an increase in antioxidant capacity driven by mitochondrial superoxide dismutase and glutathione peroxidase. When exposed to gamma irradiation, a strong oxidative stressor, males that received anoxic conditioning had lower lipid and protein oxidative damage at sexual maturity. Anoxia conditioning led to greater male sexual competitiveness compared with unconditioned males when both were irradiated, although there was no effect of anoxia conditioning on mating competitiveness in unirradiated males. Anoxia also led to higher adult emergence rates and greater flight ability in irradiation-stressed flies while preserving sterility. Thus, hormetic treatments that increased antioxidant enzyme activity also improved male performance after irradiation, suggesting that antioxidant enzymes play an important role in mediating the relationship between oxidative stress and sexual selection. Furthermore, our work has important applied implications for the sterile insect technique (SIT), an environmentally friendly method of insect pest control where males are sterilized by irradiation and deployed in the field to disrupt pest populations via mating. We suggest that hormetic treatments specifically designed to enhance antioxidant activity may produce more sexually competitive sterile males, thus improving the efficacy and economy of SIT programs.