CSP and Takeout Genes Modulate the Switch between Attraction and Repulsion during Behavioral Phase Change in the Migratory Locust

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Abstract
Behavioral plasticity is the most striking trait in locust phase transition. However, the genetic basis for behavioral plasticity in locusts is largely unknown. To unravel the molecular mechanisms underlying the behavioral phase change in the migratory locust Locusta migratoria, the gene expression patterns over the time courses of solitarization and gregarization were compared by oligonucleotide microarray analysis. Data analysis revealed that several gene categories relevant to peripheral olfactory perception are strongly regulated in a total of 1,444 differentially expressed genes during both time courses. Among these candidate genes, several CSP (chemosensory protein) genes and one takeout gene, LmigTO1, showed higher expression in gregarious and solitarious locusts, respectively, and displayed opposite expression trends during solitarization and gregarization. qRT-PCR experiments revealed that most CSP members and LmigTO1 exhibited antenna-rich expressions. RNA interference combined with olfactory behavioral experiments confirmed that the CSP gene family and one takeout gene, LmigTO1, are involved in the shift from repulsion to attraction between individuals during gregarization and in the reverse transition during solitarization. These findings suggest that the response to locust-emitted olfactory cues regulated by CSP and takeout genes is involved in the behavioral phase change in the migratory locust and provide a previously undescribed molecular mechanism linked to the formation of locust aggregations. The migratory locust, Locusta migratoria, is a worldwide agricultural pest whose outbreaks can result in plagues during which locusts mass migrate in marching bands and flying swarms. They exhibit striking phenotypic plasticity depending on the population density. They can transform between the barely-visible solitarious phase and the swarm-forming gregarious phase. A key step in the formation of large aggregation is the initial shift from the strong mutual aversion in solitarious locusts to the attraction to each other in gregarious locusts. Previous genomics studies have revealed 532 differentially expressed genes and many regulating small RNAs between the two phases of the migratory locust. Here, we developed a large-scale oligonucleotide microarray to quantify the expression of 9,154 genes during the time courses of isolating gregarious locusts and crowding solitarious locusts. We found that several olfaction-related genes, several CSPs and one takeout, are strongly regulated during both processes and display opposite expression trends in response to population density change. We then identified that these genes mediate the rapid switch of attraction/repulsion behaviors in the migratory locust. Our findings are particularly significant for understanding the process of locust aggregation and may provide new targets to manipulate locust behavior as part of novel management strategies.