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

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...

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Main Authors: Giancarlo López‐Martínez, James E. Carpenter, Stephen D. Hight, Daniel A. Hahn
Format: Article
Language:English
Published: Wiley 2021-02-01
Series:Evolutionary Applications
Subjects:
Online Access:https://doi.org/10.1111/eva.13141
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author Giancarlo López‐Martínez
James E. Carpenter
Stephen D. Hight
Daniel A. Hahn
author_facet Giancarlo López‐Martínez
James E. Carpenter
Stephen D. Hight
Daniel A. Hahn
author_sort Giancarlo López‐Martínez
collection DOAJ
description 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 1‐hr anoxic‐conditioning period (physiological conditioning hormesis) prior to and during irradiation improves male field 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 field performance and longevity in the field. Based on capture rates after a series of mark release–recapture 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 postirradiation damage and increased flight performance and recapture duration under 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.
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spelling doaj.art-db65805d52074cdaa437be01327212b92022-12-21T18:14:56ZengWileyEvolutionary Applications1752-45712021-02-0114256657610.1111/eva.13141Low‐oxygen hormetic conditioning improves field performance of sterile insects by inducing beneficial plasticityGiancarlo López‐Martínez0James E. Carpenter1Stephen D. Hight2Daniel A. Hahn3Department of Entomology and Nematology University of Florida Gainesville Florida USAUSDA‐ARS Crop Protection and Management Research Unit Tifton Georgia USAUSDA‐ARS Center for Medical, Agricultural, & Veterinary Entomology Tallahassee Florida USADepartment of Entomology and Nematology University of Florida Gainesville Florida USAAbstract 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 1‐hr anoxic‐conditioning period (physiological conditioning hormesis) prior to and during irradiation improves male field 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 field performance and longevity in the field. Based on capture rates after a series of mark release–recapture 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 postirradiation damage and increased flight performance and recapture duration under 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.https://doi.org/10.1111/eva.13141anoxiahormesismodified atmospheressterile insect technique
spellingShingle Giancarlo López‐Martínez
James E. Carpenter
Stephen D. Hight
Daniel A. Hahn
Low‐oxygen hormetic conditioning improves field performance of sterile insects by inducing beneficial plasticity
Evolutionary Applications
anoxia
hormesis
modified atmospheres
sterile insect technique
title Low‐oxygen hormetic conditioning improves field performance of sterile insects by inducing beneficial plasticity
title_full Low‐oxygen hormetic conditioning improves field performance of sterile insects by inducing beneficial plasticity
title_fullStr Low‐oxygen hormetic conditioning improves field performance of sterile insects by inducing beneficial plasticity
title_full_unstemmed Low‐oxygen hormetic conditioning improves field performance of sterile insects by inducing beneficial plasticity
title_short Low‐oxygen hormetic conditioning improves field performance of sterile insects by inducing beneficial plasticity
title_sort low oxygen hormetic conditioning improves field performance of sterile insects by inducing beneficial plasticity
topic anoxia
hormesis
modified atmospheres
sterile insect technique
url https://doi.org/10.1111/eva.13141
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AT jamesecarpenter lowoxygenhormeticconditioningimprovesfieldperformanceofsterileinsectsbyinducingbeneficialplasticity
AT stephendhight lowoxygenhormeticconditioningimprovesfieldperformanceofsterileinsectsbyinducingbeneficialplasticity
AT danielahahn lowoxygenhormeticconditioningimprovesfieldperformanceofsterileinsectsbyinducingbeneficialplasticity