Locust density shapes energy metabolism and oxidative stress resulting in divergence of flight traits

Abstract

Flight ability is essential for the enormous diversity and evolutionary success of insects. The migratory locusts exhibit flight capacity plasticity in gregarious and solitary individuals closely linked with different density experiences. However, the differential mechanisms underlying flight traits of locusts are largely unexplored. Here, we investigated the variation of flight capacity by using behavioral, physiological, and multiomics approaches. Behavioral assays showed that solitary locusts possess high initial flight speeds and short-term flight, whereas gregarious locusts can fly for a longer distance at a relatively lower speed. Metabolome–transcriptome analysis revealed that solitary locusts have more active flight muscle energy metabolism than gregarious locusts, whereas gregarious locusts show less evidence of reactive oxygen species production during flight. The repression of metabolic activity by RNA interference markedly reduced the initial flight speed of solitary locusts. Elevating the oxidative stress by paraquat injection remarkably inhibited the long-distance flight of gregarious locusts. In respective crowding and isolation treatments, energy metabolic profiles and flight traits of solitary and gregarious locusts were reversed, indicating that the differentiation of flight capacity depended on density and can be reshaped rapidly. The density-dependent flight traits of locusts were attributed to the plasticity of energy metabolism and degree of oxidative stress production but not energy storage. The findings provided insights into the mechanism underlying the trade-off between velocity and sustainability in animal locomotion and movement.

Gregarious locusts down-regulate muscular catabolic capacities yet fly far

“…Du et al. ( 2 ) find the opposite. Gregarious forms have lower levels of transcripts and maximal activities for a large number of enzymes involved in oxidative catabolism.…”

“…One of the most striking aspects of locust biology is the still poorly understood phenotypic transformation from a solitarious, nonswarming form to a gregarious, swarm-migrating form ( 1 ). Du et al.’s publication ( 2 ) in PNAS provides important insights into the mechanisms and consequences of this transformation, with insights relevant to anyone interested in performance trade-offs between speed and endurance.…”

“…However, Du et al. ( 2 ) demonstrate that solitarious, but not gregarious, locusts show evidence of redox disruption during flight, a pattern increasingly linked with muscle fatigue. After 1 h of flight, solitarious, but not gregarious, locusts showed an increase in muscle hydrogen peroxide levels and decreases in the redox scavengers xanthine, hypoxanthine, uric acid, inosinic acid, and glutathione.…”

“…Du et al. ( 2 ) hypothesize that the solitarious forms are adapted for high initial flight performance as they are likely to depend on rapid acceleration for escape from predators, perhaps a less strong selective force for gregarious forms.…”

“…Most of these experiments were conducted with locusts maintained for generations under crowded or solitary conditions, but Du et al. ( 2 ) also demonstrate that many of the same transcriptional, protein, ROS-scavenger, and behavioral patterns arose in gregarious and solitarious locusts switched and reared in solitary or crowded conditions, respectively, for 2 wk as young adults. Prior research has shown that the transformation into the gregarious form is species specific but depends on subsets of mechanosensory, visual, and/or olfactory input ( 1 , 9 ).…”