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

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.

Epigenetics and locust life phase transitions

“…In addition, it was found that fourth instar locusts displayed the most divergence between polymorphic states. This was confirmed by micro-array studies, which illustrated that the top pathways affected in gregarious nymphs at fourth stage were involved in general metabolism and catecholamine biosynthesis (Ma et al, 2011).…”

“…In addition, it was found that fourth instar locusts displayed the most divergence between polymorphic states. This was confirmed by micro-array studies, which illustrated that the top pathways affected in gregarious nymphs at fourth stage were involved in general metabolism and catecholamine biosynthesis (Ma et al, 2011).Another micro-array study on fourth instar migratory locusts during phase transition revealed differential expression in chemosensory proteins and takeout proteins (Guo et al, 2011). Genes of these families were found to be highly expressed in peripheral tissues (sensilla, antennae, labial palps, wings and hindlegs) but not internal tissues.…”

“…Another micro-array study on fourth instar migratory locusts during phase transition revealed differential expression in chemosensory proteins and takeout proteins (Guo et al, 2011). Genes of these families were found to be highly expressed in peripheral tissues (sensilla, antennae, labial palps, wings and hindlegs) but not internal tissues.…”

“…Moreover, injection of serotonin (and its analogues) is sufficient to induce gregariousness in both S. gregaria and L. migratoria, whereas injecting serotonin antagonists inhibits tactile stimulation-induced phase transition (Anstey et al, 2009;Ma et al, 2011). These observations establish serotonin as an important regulatory agent in phase transition, an effect that is probably mediated through protein kinase A signalling (Ott et al, 2012).…”

“…Pharmacological and transcriptional silencing experiments identified dopamine, in addition to serotonin, as another potent gregarisation factor in the migratory locust, driving both behavioural transition and melanin deposition (Ma et al, 2011).…”