Unveiling the mechanism by which microsporidian parasites prevent locust swarm behavior

Significance The ability of parasites to modify the behavior of their hosts is a widespread phenomenon, but the underlying mechanisms remain to be deciphered. Locusts such as Locusta migratoria manilensis are infamous for their ability to aggregate into gregarious migratory swarms that pose a major threat to food security. The microsporidian parasite Paranosema locustae can disrupt swarm formation by migratory locusts, but the underlying mechanisms of this action remain unexplored. In this study, we found that P. locustae and the native gut bacteria that produce the aggregation pheromone are mutually refractory. The reduction in aggregation pheromone reduces the production of the neurotransmitter serotonin (which initiates gregarization) and dopamine (which induces and maintains gregarization), preventing swarm behavior of migratory locusts. Locusts are infamous for their ability to aggregate into gregarious migratory swarms that pose a major threat to food security. Aggregation is elicited by an interplay of visual, tactile, and chemical stimuli, but the aggregation pheromone in feces is particularly important. Infection by the microsporidian parasite Paranosema (Nosema) locustae is known to inhibit aggregation of solitary Locusta migratoria manilensis and to induce gregarious locusts to shift back to solitary behavior. Here we suggest that P. locustae achieves this effect by acidifying the hindgut and modulating the locust immune response, which suppresses the growth of the hindgut bacteria that produce aggregation pheromones. This in turn reduces production of the neurotransmitter serotonin that initiates gregarious behavior. Healthy L. migratoria manilensis exposed to olfactory stimuli from parasite-infected locusts also produced significantly less serotonin, reducing gregarization. P. locustae also suppresses biosynthesis of the neurotransmitter dopamine that maintains gregarization. Our findings reveal the mechanisms by which P. locustae reduces production of aggregation pheromone and blocks the initiation and maintainence of gregarious behavior.

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