Unveiling the mechanism by which microsporidian parasites prevent locust swarm behavior

Abstract

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.

Microsporidia–host interactions

“…Volatiles from the feces of infected locusts were less attractive to healthy locusts than volatiles from the feces of uninfected animals. In addition to reducing the onset of aggregating behaviors, RNAseq data shows that microsporidia infection suppresses synthesis of dopamine, a neurotransmitter that helps maintain swarming [50]. This study again illustrates how far-reaching the impact of microsporidia infection can be in a host, with changes in the host microbiome due to microsporidia adversely affecting important behaviors like locust swarming.…”

“…In another fascinating example of the complex behavioral changes that can occur upon microsporidia infection, Shi et al present data for a mechanism by which microsporidia infection can prevent locust swarming [50]. In their paper, the authors propose that the locust-infecting microsporidia, Antonospora ( Nosema) locustae , acidifies the hindgut of the host locust during infection, which reduces growth of a particular commensal bacterial species that is responsible for producing pheromones that promote swarming behavior.…”

An alternative pathway to eusociality: Exploring the molecular and functional basis of fortress defense

“…We were particularly interested in the Pale mutant, because tyrosine hydroxylase catalyzes the rate‐limited step in melanin biosynthesis (Shi et al. ; the conversion of tyrosine to l ‐dopa), and occurs upstream of most of the biosynthetic steps associated with cytotoxic intermediates and free radical reactions (Nappi and Vass ). Possibly then, the general toxicity we observed is associated with more systemic deleterious effects of unchecked melanization (Sadd and Siva‐Jothy ).…”

Effect ofParanosema locustae(Microsporidia) on the behavioural phases ofLocusta migratoria(Orthoptera: Acrididae) in the laboratory

“…This may be the one of the causes of reductions in directional changes here. Shi et al (2014) systematically investigated the effect of P. locustae on phase transformations by using deep sequencing to compare the transcriptomes of healthy and infected locusts. Among the 1684 sequences that showed differential expression between the infected and uninfected locusts, 861 were up-regulated and 823 were down-regulated.…”