Juvenile hormone suppresses aggregation behavior through influencing antennal gene expression in locusts.

Wei Guo,Pengcheng Yang,Xianhui Wang,Dani Ren,Juan Song,Dafeng Chen,Xiangyong Chen,Le Kang,Lynn M Riddiford

doi:10.1371/journal.pgen.1008762

Wei Guo, Pengcheng Yang + Show 7 more

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https://doi.org/10.1371/journal.pgen.1008762

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Abstract

Animals often exhibit dramatically behavioral plasticity depending on their internal physiological state, yet little is known about the underlying molecular mechanisms. The migratory locust, Locusta migratoria, provides an excellent model for addressing these questions because of their famous phase polyphenism involving remarkably behavioral plasticity between gregarious and solitarious phases. Here, we report that a major insect hormone, juvenile hormone, is involved in the regulation of this behavioral plasticity related to phase change by influencing the expression levels of olfactory-related genes in the migratory locust. We found that the treatment of juvenile hormone analog, methoprene, can significantly shift the olfactory responses of gregarious nymphs from attraction to repulsion to the volatiles released by gregarious nymphs. In contrast, the repulsion behavior of solitarious nymphs significantly decreased when they were treated with precocene or injected with double-stranded RNA of JHAMT, a juvenile hormone acid O-methyltransferase. Further, JH receptor Met or JH-response gene Kr-h1 knockdown phenocopied the JH-deprivation effects on olfactory behavior. RNA-seq analysis identified 122 differentially expressed genes in antennae after methoprene application on gregarious nymphs. Interestingly, several olfactory-related genes were especially enriched, including takeout (TO) and chemosensory protein (CSP) which have key roles in behavioral phase change of locusts. Furthermore, methoprene application and Met or Kr-h1 knockdown resulted in simultaneous changes of both TO1 and CSP3 expression to reverse pattern, which mediated the transition between repulsion and attraction responses to gregarious volatiles. Our results suggest the regulatory roles of a pleiotropic hormone in locust behavioral plasticity through modulating gene expression in the peripheral olfactory system.

Highlights

Insects generally express behavioral plasticity to adapt environmental changes by integrating precisely internal and external chemical cues
We investigated the effect of juvenile hormone (JH) on the behavioral transition in fourth-instar gregarious and solitarious locusts
We found that JH induced the behavioral shift of the gregarious locust from attraction to repulsion to the volatiles of gregarious locusts

Summary

Introduction

Insects generally express behavioral plasticity to adapt environmental changes by integrating precisely internal and external chemical cues. Gregarious locusts in high density actively aggregate; solitarious locusts at low density are shy and actively avoid each other This attraction/repulsion behavior of locusts has been demonstrated to be induced exclusively by conspecific olfactory cues [9,10,11,12,13]. The shift between attractive and repulsive responses to olfactory cues can occur rapidly within several hours with changes in population density [14, 15]. Our previous studies have revealed that the detailed regulatory mechanisms underlying phase-dependent olfactory-mediated behavioral plasticity occurred at the central nervous system (CNS), including several monoamine signaling pathways [6]. The invertebrate-specific octopamine-OARa and tyramine-TAR signaling pathways are involved in the regulation of attractive and repulsive behavior probably in the primary olfactory center of the L. migratoria [14]. An understanding of global regulatory factors remains largely unknown at the peripheral olfactory system level

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