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Enhanced immune responses of gregarious larvae contribute to successful adult migration in the migratory oriental armyworm

Hailong Kong1, 2*#, Dong Guo1*, Lei Zhang1*, Dianjie Xie1, Kenneth Wilson3, Xingfu Jiang1#

1 State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China

2 College of Plant Protection, Yangzhou University, Yangzhou 225009, China

3 Lancaster Environment Centre, Lancaster University, Lancaster LA1 4YQ, UK 

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摘要  

迁飞性昆虫害虫通常会在短时间内迁入到新的栖息地,很快同步产卵导致幼虫聚集,对作物造成严重为害。聚集幼虫能很好地适应新栖息地的天敌或病原物,但它们如何增强抗病性和免疫的生物学意义尚不清楚。本文研究了病原物和寄生蝇的感染,如何影响群居型和散居型粘虫幼虫的免疫反应和成虫的迁飞行为。结果表明,与散居型幼虫相比,群居型幼虫对白僵菌和伞裙追寄蝇的抵抗能力明显提高。白僵菌侵染后,群居型幼虫的酚氧化酶活性和溶菌酶活性比散居型的明显增强,同时群居型幼虫的多巴胺和5-羟色胺水平也明显增加。注射外源多巴胺(或5-羟色胺)后,幼虫的酚氧化酶活性、溶菌酶活性、抗菌活性和幼虫存活率均明显提高。同时,被白僵菌感染的群居型幼虫发育的成虫飞行能力显著提高,然而,被感染的散居型幼虫发育的成虫飞行能力无明显变化。另外,被感染的群居型和散居型幼虫发育的成虫产卵前期、产卵历期和产卵量均无显著影响。这些结果为阐明成虫迁飞与幼虫免疫之间的关系以及免疫后行为学后果提供了新的见解。



Abstract  

Migratory insect pests tend to suddenly immigrate into new habitats over a short period to simultaneously lay eggs in clusters, resulting in gregarious larvae that cause severe damage to crops. These aggregated larvae can adapt well to various natural enemies and pathogens in their new habitats, but how their resistance might be enhanced and its immunological significance remain unknown. Here, we examined how infection by a pathogen and a parasitic fly affect the immune response and migratory behavior in two phases of the oriental armyworm, Mythimna separata, which differ dramatically in their flight capacity and fecundity. The gregarious larvae displayed greater resistance than solitary larvae to the challenges of both the entomopathogenic fungus Metarhizium anisopliae and the parasitoid Exorista civilis. In response to a challenge by M. anisopliae, gregarious larvae exhibited more pronounced increases in phenoloxidase (PO) activity and lysozyme activity than solitary larvae. Furthermore, in addition to the greater PO and lysozyme activities, the levels of dopamine and 5-hydroxytryptamine (5-HT) were also greater in challenged gregarious and solitary larvae. Injection of dopamine (or 5-HT) significantly enhanced PO activity, lysozyme activity, antibacterial activity and larval survival. Subsequently, there was a significant increase in the flight capacity of adults derived from gregarious larvae challenged by M. anisopliae; while no significant variation was observed in the adults from challenged solitary larvae. The preoviposition period, oviposition period and fecundity were not significantly affected by M. anisopliae, regardless of whether the larvae were gregarious or solitary. These results provide new insights into the relationship between migration and immunity in insects, and their behavior after immunization.

Keywords:  gregariousness       immunity        migration        neurohormone        Mythimna separata  
Online: 10 February 2025  
Fund: 

This work was supported by the National Key Research and Development Program of China (2022YFD1400600), the National Natural Science Foundation of China (32172397, 32472540,31871951 and 31672019), the China Agriculture Research System of MOF and MARA (CARS-22) and the Natural Science Foundation of Beijing, China (6172030).

About author:  #Correspondence Xingfu Jiang, E-mail: xfjiang@ippcaas.cn; Hailong Kong, E-mail: khl2504@126.com *These authors contributed equally to this study.

Cite this article: 

Hailong Kong, Dong Guo, Lei Zhang, Dianjie Xie, Kenneth Wilson, Xingfu Jiang. 2025. Enhanced immune responses of gregarious larvae contribute to successful adult migration in the migratory oriental armyworm. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2025.02.003

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