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

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.

Phase-related differences in egg production of the migratory locust regulated by differential oosorption through microRNA-34 targeting activinβ

Outbreaks of locust plagues result from the long-term accumulation of high-density egg production. The migratory locust, Locusta migratoria, displays dramatic differences in the egg-laid number with dependence on population density, while solitarious locusts lay more eggs compared to gregarious ones. However, the regulatory mechanism for the egg-laid number difference is unclear. Herein, we confirm that oosorption plays a crucial role in the regulation of egg number through the comparison of physiological and molecular biological profiles in gregarious and solitarious locusts. We find that gregarious oocytes display a 15% higher oosorption ratio than solitarious ones. Activinβ (Actβ) is the most highly upregulated gene in the gregarious terminal oocyte (GTO) compared to solitarious terminal oocyte (STO). Meanwhile, Actβ increases sharply from the normal oocyte (N) to resorption body 1 (RB1) stage during oosorption. The knockdown of Actβ significantly reduces the oosorption ratio by 13% in gregarious locusts, resulting in an increase in the egg-laid number. Based on bioinformatic prediction and experimental verification, microRNA-34 with three isoforms can target Actβ. The microRNAs display higher expression levels in STO than those in GTO and contrasting expression patterns of Actβ from the N to RB1 transition. Overexpression of each miR-34 isoform leads to decreased Actβ levels and significantly reduces the oosorption ratio in gregarious locusts. In contrast, inhibition of the miR-34 isoforms results in increased Actβ levels and eventually elevates the oosorption ratio of solitarious locusts. Our study reports an undescribed mechanism of oosorption through miRNA targeting of a TGFβ ligand and provides new insights into the mechanism of density-dependent reproductive adaption in insects.

Linseed Oil Affects Aggregation Behaviour in the Desert Locust Schistocerca gregaria—A Potential Swarm Disruptive Agent

Gregarious desert locusts constitute very destructive agricultural pests. They aggregate and form collectively moving swarms that devastate vegetation and reduce crop production. To combat gregarious locusts, a bio-pesticide formulation that contains linseed oil as the main component was described recently. Since linseed oil is rich in fatty acids, some of which function as necromones that indicate injury or death in various insect species, we investigated the influence of linseed oil on the aggregation behaviour of sexually mature gregarious desert locusts. For this reason, we performed a series of aggregation experiments with six individuals of the same sex and brushed the wings of one individual (target individual) with linseed oil. The time the oil brushed target males spent close to any other individual was reduced in 76% of trials (average reduction of 18%), whereas the time target females spent in groups with members of the same sex did not alter. These results suggest that linseed oil may act as a bioactive agent that has the potential to disrupt swarm formation.

SURVIVAL OF MIGRATORY LOCUST AT DIFFERENT KEEPING CONDITIONS

In this article we studied the conditions for keeping two species of gregarious locusts: the African migratory locust (Locusta migratoria migratorioides) and the Asian migratory locust (Locusta migratoria migratoria) in open and shaded areas. Based on the data obtained, it is shown that the survival rate of insects of the non-diapausal subspecies was higher in comparison with the obligate monovoltine.

A β-carotene-binding protein carrying a red pigment regulates body-color transition between green and black in locusts

Changes of body color have important effects for animals in adapting to variable environments. The migratory locust exhibits body color polyphenism between solitary and gregarious individuals, with the former displaying a uniform green coloration and the latter having a prominent pattern of black dorsal and brown ventral surface. However, the molecular mechanism underlying the density-dependent body color changes of conspecific locusts remain largely unknown. Here, we found that upregulation of β-carotene-binding protein promotes the accumulation of red pigment, which added to the green color palette present in solitary locusts changes it from green to black, and that downregulation of this protein led to the reverse, changing the color of gregarious locusts from black to green. Our results provide insight that color changes of locusts are dependent on variation in the red β-carotene pigment binding to βCBP. This finding of animal coloration corresponds with trichromatic theory of color vision.

Phenylacetonitrile in locusts facilitates an antipredator defense by acting as an olfactory aposematic signal and cyanide precursor

Many aggregating animals use aposematic signals to advertise their toxicity to predators. However, the coordination between aposematic signals and toxins is poorly understood. Here, we reveal that phenylacetonitrile (PAN) acts as an olfactory aposematic signal and precursor of hypertoxic hydrogen cyanide (HCN) to protect gregarious locusts from predation. We found that PAN biosynthesis from phenylalanine is catalyzed byCYP305M2, a novel gene encoding a cytochrome P450 enzyme in gregarious locusts. The RNA interference (RNAi) knockdown ofCYP305M2increases the vulnerability of gregarious locusts to bird predation. By contrast, the elevation of PAN levels through supplementation with synthetic PAN increases the resistance of solitary locusts to predation. When locusts are attacked by birds, PAN is converted to HCN, which causes food poisoning in birds. Our results indicate that locusts develop a defense mechanism wherein an aposematic compound is converted to hypertoxic cyanide in resistance to predation by natural enemies.

Red and black: A β-carotene-binding protein carrying a red pigment regulates body-color transition in locusts

Changes of body color have important effects for animals in adapting to variable environments. The migratory locust exhibits body color polyphenism between solitary and gregarious individuals, with the former displaying a uniform green coloration and the latter having a prominent pattern of black dorsal and brown ventral surface. However, the molecular mechanism underlying the density-dependent body color changes of conspecific locusts remain largely unknown. Here, we found that up regulation of β-carotene-binding protein promotes the accumulation of red pigment, which added to the green color palette present in solitary locusts changes it from green to black, and that down regulation of this protein led to the reverse, changing the color of gregarious locusts from black to green. Our results provide insight that color changes of locusts are dependent on variation in the red β-carotene pigment binding to βCBP. This finding of animal coloration corresponds with trichromatic theory of color vision.

Sexual behavior of the desert locust during intra-and inter-phase interactions

Mating and reproduction behaviors and strategies are fundamental aspects of an organism’s evolutionary and ecological success. In locusts, intra- as well as inter-phase reproductive interactions among gregarious and solitarious locust populations have a major impact on the locust population dynamics. However, practically all previous work on locust sexual behavior has been limited to the gregarious phase. Here we provide a first detailed description of pre-copulatory behavior of solitarious desert locusts. We compare our findings with those of previous reports of pre-copulatory behavior of gregarious locusts, focusing on the behavioral elements that serve in inter-sex signaling and communication. We also studied inter-phase (mixed pairs) reproductive interactions. Solitarious males were found to invest more in pre-copulatory courtship and signaling compared to their gregarious counterparts; and the solitarious females played a comparatively more dominant role in the inter-sex communication. The solitarious females were also less prone to demonstrate the typical rejection-related behavioral patterns displayed by the gregarious females. As a consequence of the particular characteristic behavior of each phase, the most successful among intra- and inter-phase pairs were gregarious males with solitary females. Least successful were solitary males encountered with gregarious females, indicating a strong asymmetry in inter-phase reproductive interactions. We discuss these results in the context of non-random or assortative mating in locust mixed or sympatric solitarious-gregarious populations.

MicroRNA-276 promotes egg-hatching synchrony by up-regulating brm in locusts

Developmental synchrony, the basis of uniform swarming, migration, and sexual maturation, is an important strategy for social animals to adapt to variable environments. However, the molecular mechanisms underlying developmental synchrony are largely unexplored. The migratory locust exhibits polyphenism between gregarious and solitarious individuals, with the former displaying more synchronous sexual maturation and migration than the latter. Here, we found that the egg-hatching time of gregarious locusts was more uniform compared with solitarious locusts and that microRNA-276 (miR-276) was expressed significantly higher in both ovaries and eggs of gregarious locusts than in solitarious locusts. Interestingly, inhibiting miR-276 in gregarious females and overexpressing it in solitarious females, respectively, caused more heterochronic and synchronous hatching of progeny eggs. Moreover, miR-276 directly targeted a transcription coactivator gene, brahma (brm), resulting in its up-regulation. Knockdown of brm not only resulted in asynchronous egg hatching in gregarious locusts but also impaired the miR-276–induced synchronous egg hatching in solitarious locusts. Mechanistically, miR-276 mediated brm activation in a manner that depended on the secondary structure of brm, namely, a stem-loop around the binding site of miR-276. Collectively, our results unravel a mechanism by which miR-276 enhances brm expression to promote developmental synchrony and provide insight into regulation of developmental homeostasis and population sustaining that are closely related to biological synchrony.