Overexpression of an antioxidant enzyme improves male mating performance after stress in a lek-mating fruit fly

Authors: TEETS, NICHOLAS - University Of Kentucky; DIAS, VANESSA - University Of Florida; PIERCE, BAILEY - University Of Florida; SCHETELIG, MARC - Justus-Liebig University; Handler, Alfred - Al; HAHN, DANIEL - University Of Florida

Submitted to: Proceedings of the Royal Society B
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/21/2019
Publication Date: 6/12/2019
Citation: Teets, N.M., Dias, V., Pierce, B., Schetelig, M.F., Handler, A.M., Hahn, D.A. 2019. Overexpression of an antioxidant enzyme improves male mating performance after stress in a lek-mating fruit fly. Proceedings of the Royal Society B. 286(1904):20190898. https://doi.org/10.1098/rspb.2019.0531.
DOI: https://doi.org/10.1098/rspb.2019.0531

Interpretive Summary: A major impediment to effective Sterile Insect Technique (SIT) is the reduction of the sexual competitiveness, general fitness and longevity of irradiated males. Insects, as well as many other organisms, respond to stressors such as irradiation by using antioxidant enzymes to reduce oxidative damage. To further understand this response and possibly increase the insects’ capacity to reduce this damage, scientists at USDA-ARS, Center for Medical, Agricultural and Veterinary Entomology, Gainesville, Florida, and collaborators at the University of Florida and the Justus-Liebig-University Giessen, Germany, report experiments on genetic modifications resulting in the overproduction for a key antioxidant enzyme gene in the Caribbean fruit fly. This was achieved by using genetic transformation to introduce additional gene copies in this agricultural pest. Adult males from these strains were then sterilized by irradiation and tested for longevity, male sexual performance and locomotor activity compared to non-sterilized wild type males. For two of the overproduction lines, improved mating performance and locomotor activity was observed, as well as a reduction in oxidative damage to lipids. These results show a clear link between oxidative stress, antioxidant capacity and male performance, indicating promise for the use of transgenic approaches to enhance the efficacy of male insects released for area-wide pest management programs.

Technical Abstract: Many environmental stressors generate reactive oxygen species, and ecological evidence indicates that key life history traits such as mating performance and longevity are mediated by oxidative stress. For insects used in Sterile Insect Technique (SIT), oxidative damage caused by sterilizing radiation reduces the competitiveness and ultimately economic efficiency of released males. Here, we test the hypothesis that transgenic overexpression of a key antioxidant enzyme reduces oxidative damage and enhances mating performance in the context of SIT. We generated seven transgenic lines of the Caribbean fruit fly, Anastrepha suspensa that overexpress mitochondrial superoxide dismutase (MnSOD), a key antioxidant enzyme that metabolizes damaging superoxide radicals. After sterilization by irradiation, two of the lines with intermediate MnSOD overexpression showed enhanced mating performance relative to sterilized wild type males. In contrast, the transgene did not improve longevity, and most lines had shorter lifespans than wild type. For the two lines with improved mating performance, MnSOD overexpression also preserved locomotor activity, as indicated by a laboratory climbing assay. In these two lines, improvements in mating performance and climbing corresponded with a reduction in oxidative damage to lipids, indicating that MnSOD overexpression protects flies from oxidative stress at the cellular level. Taken together, our results show a clear link between oxidative stress, antioxidant capacity and male performance, and our work shows promise for using transgenic approaches to enhance the efficacy of insects released as components of area-wide pest management strategies.