Mitochondrial superoxide dismutase overexpression and low oxygen conditioning hormesis improve the performance of irradiated sterile males

Authors: DIAS, VANESSA - International Atomic Energy Agency (IAEA); CACERES, CARLOS - International Atomic Energy Agency (IAEA); PARKER, ANDREW - International Atomic Energy Agency (IAEA); PEREIRA, RUI - International Atomic Energy Agency (IAEA); DEMIRBAS-UZEL, GULER - International Atomic Energy Agency (IAEA); ABD-ALLA, ADLY - International Atomic Energy Agency (IAEA); TEETS, NICHOLAS - University Of Kentucky; SCHETELIG, MARC - Justus-Liebig University; Handler, Alfred - Al; HAHN, DANIEL - University Of Florida

Submitted to: Scientific Reports
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/29/2021
Publication Date: 10/12/2021
Citation: Dias, V.S., Caceres, C., Parker, A.G., Pereira, R., Demirbas-Uzel, G., Abd-Alla, A.M., Teets, N.M., Schetelig, M.F., Handler, A.M., Hahn, D.A. 2021. Mitochondrial superoxide dismutase overexpression and low oxygen conditioning hormesis improve the performance of irradiated sterile males. Scientific Reports. 11. Article 20182. https://doi.org/10.1038/s41598-021-99594-1.
DOI: https://doi.org/10.1038/s41598-021-99594-1

Interpretive Summary: The Sterile Insect Technique (SIT) uses ionizing radiation to reduce populations of insect pests like the Caribbean fruit fly by rearing large numbers of males, exposing them to radiation, and then releasing them to mate with native females who then fail to reproduce. Often, the sterile males compete less effectively than native males in finding mates because radiation can damage their protective antioxidant enzymes in addition to causing sterility. To further understand this damage and possibly increase the insects’ capacity to repair it, scientists at USDA-ARS, Center for Medical, Agricultural and Veterinary Entomology, Gainesville, Florida, and collaborators at the International Atomic Energy Agency (IAEA), the University of Florida and the Justus-Liebig-University Giessen, Germany, conducted experiments to create a strain of fruit flies that overproduced a key antioxidant enzyme. Irradiated adult males from these strains were then tested to consider the role of protective antioxidants in physiological health and sexual behavior. Our results showed that overexpression of one antioxidant enzyme, SOD2, provides improvements in the health and sexual behavior of irradiated males. The study provides valuable new information for improving the quality and sexual behavior of sterile males used in SIT programs.

Technical Abstract: The Sterile Insect Technique (SIT) is a successful autocidal control method that uses ionizing radiation to sterilize insects. Unfortunately, irradiation in normal atmospheric conditions can be damaging for males, because it generates substantial oxidative stress that, combined with mass-rearing conditions, may reduce their sexual competitiveness and quality. In this study, oxidative stress and antioxidant capacity were experimentally manipulated in Anastrepha suspensa using a combination of low-oxygen conditions and transgenic overexpression of mitochondrial superoxide dismutase (SOD2) to evaluate the role of oxidative stress and cellular antioxidants in the sexual behavior and quality of irradiated males. Our results showed that SOD2 overexpression enhances irradiated insect quality and improves male competitiveness in leks. However, the improvements in mating performance were modest, as normoxia-irradiated SOD2 males exhibited a 22% improvement in mating success compared to normoxia-irradiated wild type males. Additionally, SOD2 overexpression did not synergistically improve the mating success of males irradiated in either hypoxia or severe hypoxia. Short-term hypoxic and severe-hypoxic conditioning hormesis, per se, increased antioxidant capacity and enhanced sexual competitiveness of irradiated males relative to non-irradiated males in leks. Our study provides valuable new information that antioxidant enzymes, particularly SOD2, have potential to improve the quality and lekking performance of sterile males used in SIT programs.