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

PLoS Genet. 2020 Apr 29;16(4):e1008762. doi: 10.1371/journal.pgen.1008762. eCollection 2020 Apr.

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Arthropod Antennae / drug effects
  • Arthropod Antennae / metabolism*
  • Behavior, Animal / drug effects*
  • Genes, Insect
  • Grasshoppers
  • Insect Proteins / genetics
  • Insect Proteins / metabolism
  • Juvenile Hormones / pharmacology*
  • Methoprene / pharmacology
  • Methyltransferases / genetics
  • Methyltransferases / metabolism
  • Social Behavior*
  • Transcriptome / drug effects*

Substances

  • Insect Proteins
  • Juvenile Hormones
  • Methoprene
  • Methyltransferases

Grants and funding

National Natural Science Foundation of China (No. 31210103915 to LK, No. 31930012 and No. 31772531 to XW), and the Youth Innovation Promotion Association, CAS (No. 2016080 to WG). http://www.nsfc.gov.cn/english/site_1/http://www.yicas.cn/portal.php The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.