Indirect and direct interactions between grain aphid and parasitoid in the presence of symbiont Regiella insecticola

Abstract Background Aphids often harbor bacterial symbionts that confer resistance to biotic and abiotic stress. Previous studies have primarily examined the direct effects of symbiont infection on parasitoid success but less on aphid population dynamics under indirect parasitic situations, for exam...

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Main Authors: Yue Man, Delu Li, Minghui Wang, Zuqing Hu, Jean-Luc Gatti, Nicolas Desneux, Peng Han, Chen Luo
Format: Article
Language:English
Published: CABI 2023-12-01
Series:CABI Agriculture and Bioscience
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Online Access:https://doi.org/10.1186/s43170-023-00202-1
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author Yue Man
Delu Li
Minghui Wang
Zuqing Hu
Jean-Luc Gatti
Nicolas Desneux
Peng Han
Chen Luo
author_facet Yue Man
Delu Li
Minghui Wang
Zuqing Hu
Jean-Luc Gatti
Nicolas Desneux
Peng Han
Chen Luo
author_sort Yue Man
collection DOAJ
description Abstract Background Aphids often harbor bacterial symbionts that confer resistance to biotic and abiotic stress. Previous studies have primarily examined the direct effects of symbiont infection on parasitoid success but less on aphid population dynamics under indirect parasitic situations, for example when exposed to parasitoid wasp odor. Deciphering this type of indirect effect is essential for understanding dynamics of insect ecosystems and communities and to improve IPM success. Methods We generated Sitobion avenae aphid clonal lines that are genetically identical but differ in Regiella insecticola infection. Then, the indirect odor effect of female parasitoid wasp Aphidius gifuensis (Ashmaed), one of its major natural enemies in the fields, was examined on the aphid lines fitness using different parasitoid densities. With these lines we also tested the direct effect of symbiont presence on aphid resistance against different parasitoid densities. Results Our study found fitness costs for the aphid line hosting Regiella, mainly via an increase in the development time and a reduction in population increase rate. Some of these fitness traits were influenced by the indirect exposure to parasitoid wasp odor with a density effect. Presence of the symbiont also reduced A. gifuensis parasitic success, increased the wasp development time and decreased its emergence weight with low effect of the parasitoid density used for parasitism. Conclusions These results showed that aphid population dynamic was mainly affected by the symbiont presence, but not by parasitoid odor. Symbiont presence also protected aphid from parasitism and affected parasitoid offspring weight and hence their future individual fertility and fitness.
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spelling doaj-art-1e86b1b4d92c470e85ece1f88eed38142025-02-03T10:34:08ZengCABICABI Agriculture and Bioscience2662-40442023-12-01411910.1186/s43170-023-00202-1Indirect and direct interactions between grain aphid and parasitoid in the presence of symbiont Regiella insecticolaYue Man0Delu Li1Minghui Wang2Zuqing Hu3Jean-Luc Gatti4Nicolas Desneux5Peng Han6Chen Luo7State Key Laboratory of Crop Stress Biology for Arid Areas, Key Laboratory of Plant Protection Resources and Pest Management of Ministry of Education, Key Laboratory of Integrated Pest Management On the Loess Plateau of Ministry of Agriculture and Rural Affairs, College of Plant Protection, Northwest A&F UniversityState Key Laboratory of Crop Stress Biology for Arid Areas, Key Laboratory of Plant Protection Resources and Pest Management of Ministry of Education, Key Laboratory of Integrated Pest Management On the Loess Plateau of Ministry of Agriculture and Rural Affairs, College of Plant Protection, Northwest A&F UniversityInstitute of Biodiversity, School of Ecology and Environmental Science, Yunnan UniversityState Key Laboratory of Crop Stress Biology for Arid Areas, Key Laboratory of Plant Protection Resources and Pest Management of Ministry of Education, Key Laboratory of Integrated Pest Management On the Loess Plateau of Ministry of Agriculture and Rural Affairs, College of Plant Protection, Northwest A&F UniversityUniversité Côte d’Azur, INRAE, CNRS, UMR-ISAUniversité Côte d’Azur, INRAE, CNRS, UMR-ISAInstitute of Biodiversity, School of Ecology and Environmental Science, Yunnan UniversityState Key Laboratory of Crop Stress Biology for Arid Areas, Key Laboratory of Plant Protection Resources and Pest Management of Ministry of Education, Key Laboratory of Integrated Pest Management On the Loess Plateau of Ministry of Agriculture and Rural Affairs, College of Plant Protection, Northwest A&F UniversityAbstract Background Aphids often harbor bacterial symbionts that confer resistance to biotic and abiotic stress. Previous studies have primarily examined the direct effects of symbiont infection on parasitoid success but less on aphid population dynamics under indirect parasitic situations, for example when exposed to parasitoid wasp odor. Deciphering this type of indirect effect is essential for understanding dynamics of insect ecosystems and communities and to improve IPM success. Methods We generated Sitobion avenae aphid clonal lines that are genetically identical but differ in Regiella insecticola infection. Then, the indirect odor effect of female parasitoid wasp Aphidius gifuensis (Ashmaed), one of its major natural enemies in the fields, was examined on the aphid lines fitness using different parasitoid densities. With these lines we also tested the direct effect of symbiont presence on aphid resistance against different parasitoid densities. Results Our study found fitness costs for the aphid line hosting Regiella, mainly via an increase in the development time and a reduction in population increase rate. Some of these fitness traits were influenced by the indirect exposure to parasitoid wasp odor with a density effect. Presence of the symbiont also reduced A. gifuensis parasitic success, increased the wasp development time and decreased its emergence weight with low effect of the parasitoid density used for parasitism. Conclusions These results showed that aphid population dynamic was mainly affected by the symbiont presence, but not by parasitoid odor. Symbiont presence also protected aphid from parasitism and affected parasitoid offspring weight and hence their future individual fertility and fitness.https://doi.org/10.1186/s43170-023-00202-1Parasitoid indirect effectSymbiont-conferred resistancePopulation dynamicAphidsAphidius gifuensis
spellingShingle Yue Man
Delu Li
Minghui Wang
Zuqing Hu
Jean-Luc Gatti
Nicolas Desneux
Peng Han
Chen Luo
Indirect and direct interactions between grain aphid and parasitoid in the presence of symbiont Regiella insecticola
CABI Agriculture and Bioscience
Parasitoid indirect effect
Symbiont-conferred resistance
Population dynamic
Aphids
Aphidius gifuensis
title Indirect and direct interactions between grain aphid and parasitoid in the presence of symbiont Regiella insecticola
title_full Indirect and direct interactions between grain aphid and parasitoid in the presence of symbiont Regiella insecticola
title_fullStr Indirect and direct interactions between grain aphid and parasitoid in the presence of symbiont Regiella insecticola
title_full_unstemmed Indirect and direct interactions between grain aphid and parasitoid in the presence of symbiont Regiella insecticola
title_short Indirect and direct interactions between grain aphid and parasitoid in the presence of symbiont Regiella insecticola
title_sort indirect and direct interactions between grain aphid and parasitoid in the presence of symbiont regiella insecticola
topic Parasitoid indirect effect
Symbiont-conferred resistance
Population dynamic
Aphids
Aphidius gifuensis
url https://doi.org/10.1186/s43170-023-00202-1
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