Low-oxygen hormetic conditioning improves field performance of sterile insects by inducing beneficial plasticity

Authors: LOPEZ-MARTINEZ, GIANCARLO - North Dakota State University; Carpenter, James; Hight, Stephen; HAHN, DANIEL - University Of Florida

Submitted to: Evolutionary Applications
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/16/2020
Publication Date: 9/28/2020
Citation: Lopez-Martinez, G., Carpenter, J.E., Hight, S.D., Hahn, D.A. 2020. Low-oxygen hormetic conditioning improves field performance of sterile insects by inducing beneficial plasticity. Evolutionary Applications. 14:566-576. https://doi.org/10.1111/eva.13141.
DOI: https://doi.org/10.1111/eva.13141

Interpretive Summary: A highly effective component of Insect Pest Management (IPM) programs is the use of Sterile Insect Technique (SIT) where laboratory-reared males of the pest insect are sterilized by irradiation and then released into the environment to mate with wild females, causing them to lay infertile eggs. Irradiation can harm the performance of the sterilized males in their ability to survive, fly, and locate female mates. To find conditions that improve male performance, scientists at USDA, Agricultural Research Service, Center for Medical, Agricultural and Veterinary Entomology, Tallahassee, Florida, and Crop Protection and Management Research Unit in Tifton, Georgia, collaborated with those at the University of Florida and North Dakota State University to conduct a laboratory study with irradiated Argentine cactus moths, an invasive pest of cactus in the U.S.A. A short period of oxygen starvation, anoxia, before and during the irradiation period of the male moths, improved their performance in field conditions. Anoxia treated, irradiated moths were active longer, flew farther, and flew in a larger area than moths that were not starved for oxygen. This method of incorporating anoxia with irradiation can lead to improved performance of the males, increase the level of control of pest populations, and save costs by producing healthier and stronger sterile insects.

Technical Abstract: As part of Sterile Insect Technique (SIT) programs, irradiation can effectively induce sterility in insects by damaging germline genomic DNA. However, irradiation also induces other off-target side effects that reduce the quality and performance of sterilized males, including the formation of damaging free radicals that can reduce sterile male performance. Thus, treatments that reduce off-target effects of irradiation on male performance while maintaining sterility can improve the feasibility and economy of SIT programs. We previously found that inducing a form of rapid, beneficial plasticity with a one-hour anoxic conditioning period (physiological conditioning hormesis) prior to and during irradiation improves male performance in the laboratory while maintaining sterility in males of the cactus moth, Cactoblastis cactorum. Here we extend this work by testing the extent to which this beneficial plasticity may improve male performance in the field. Based on capture rates after a series of mark and release experiments, we found that anoxia-conditioned irradiated moths were active in the field longer than their irradiated counterparts. In addition, anoxia-conditioned moths were captured in traps that were farther away from the release site than unconditioned moths, suggesting greater dispersal. These data confirmed that beneficial plasticity induced by anoxia hormesis prior to irradiation led to lower post-irradiation damage and increased performance beyond the laboratory in real-world field conditions. We recommend greater consideration of beneficial plasticity responses in biological control programs, and specifically the implementation of anoxia-conditioning treatments applied prior to irradiation in area-wide integrated pest management programs that use SIT.