The desert locust demonstrates density-dependent phase polyphenism: For extended periods it appears in a non-aggregating, non-migrating phenotype, known as the solitary phase. When circumstances change, solitary individuals may aggregate and transform to the gregarious phenotype, which have a strong propensity for generating large swarms. Previous reports have suggested a role for gut-bacteria derived volatiles in the swarming phenomenon, and suggested that locusts are capable of manipulating their gut microbiome according to their density-dependent phases. Here, we directly tested this hypothesis for the first time. Using locusts of both phases from well-controlled laboratory cultures as well as gregarious field-collected individuals; and high-throughput sequencing. We characterized the hindgut bacterial community composition in the two phases of the desert locust. Our findings demonstrate that laboratory-reared gregarious and solitary locusts maintain a stable core of Enterobacter. However, while different generations of gregarious locust experience shifts in their Enterobacter’s relative abundance; the solitary locusts maintain a stable gut microbiome, highly similar to that of the field-collected locusts. Tentative phase differences in wild populations’ microbiome may thus be an indirect effect of environmental or other factors that push the swarming individuals to homogenous gut bacteria. We therefore conclude that there are phase-related differences in the population dynamics of the locust hindgut bacterial composition, but there is no intrinsic density-dependent mechanism directly affecting the gut microbiome.

As one of the world’s most infamous agricultural pests, locusts have been subjected to many in-depth studies. Their ability at one end of their behavioral spectrum to live as solitary individuals under specific conditions, and at the other end of the spectrum to form swarms of biblical scale, has placed them at the focus of vast research efforts. One important aspect of locust ecology is that of their interactions with the bacteria that reside in and on them. Although this aspect of locust ecology has been little studied relative to the mainstream locust research, these bacteria have been shown both to affect locust immunity and to participate in maintaining swarm integrity through the secretion of attractant volatiles. The interaction between locusts and their bacteria seems, however, to be bi-directional, with the bacteria themselves, as recently shown, being influenced by their host’s swarming tendencies. This seems to be a consequence of the bacterial composition in the locust’s gut, reproductive organs, and integument undergoing change with the change in their host’s behavior. In this review we describe the current state of knowledge of the locust–bacteria interactions (data exists mainly for the desert and the migratory locusts), as well as highlighting some newly-gained understanding; and offer perspectives for future research.

The important role that locust gut bacteria play in their host biology is well accepted. Among other roles, gut bacteria are suggested to be involved in the locust swarming phenomenon. In addition, in many insect orders, the reproductive system is reported to serve as a vector for trans-generation bacterial inoculation. Knowledge of the bacterial composition of the locust reproductive tract is, however, practically absent. Here we characterized the reproductive system bacterial composition of gregarious and solitary females. We investigated its temporal dynamics and how it interacts with the locust phase, by comparative sampling and 16S rRNA amplicon sequencing. We revealed that the bacterial composition of the locust female reproductive tract is mostly constructed of three core genera: Micrococcus, Acinetobacter and Staphylococcus. While solitary females maintained a consistent bacterial composition, in the gregarious phase this consortium demonstrated large temporal shifts, mostly manifested by Brevibacterium blooms. These data are in accord with our previous report on the dynamics of locust hindgut bacterial microbiota, further indicating that locust endosymbionts are affected by their host population density. These newly understood dynamics may have implications beyond their contribution to our knowledge of locust ecology, as aggregation and mass migration are prevalent phenomena across many migrating animals.

A hallmark of the desert locust’s ancient and deserved reputation as a devastating agricultural pest is that of the long-distance, multi-generational migration of locust swarms to new habitats. The bacterial symbionts that reside within the locust gut comprise a key aspect of its biology, augmenting its immunity and having also been reported to be involved in the swarming phenomenon through the emission of attractant volatiles. However, it is still unclear whether and how these beneficial symbionts are transmitted vertically from parent to offspring. Using comparative 16S rRNA amplicon sequencing and direct experiments with engineered bacteria, we provide here evidence of the vertical transmission of locust gut bacteria. The females perform this activity by way of inoculation of the egg-pod’s foam plug, through which the larvae pass upon hatching. Furthermore, analysis of the biochemical structure of the foam revealed chitin to be its major component, along with immunity-related proteins such as lysozyme, which could be responsible for the inhibition of some bacteria in the foam while allowing other, more beneficial, strains to proliferate. Our findings reveal a potential vector for the transgenerational transmission of symbionts in locusts, which contributes to the locust swarm’s ability to invade and survive in new territories.

Summary A hallmark of the desert locust's ancient and deserved reputation as a devastating agricultural pest is that of the long‐distance, multi‐generational migration of locust swarms to new habitats. The bacterial symbionts that reside within the locust gut comprise a key aspect of its biology, augmenting its immunity and having also been reported to be involved in the swarming phenomenon through the emission of attractant volatiles. However, it is still unclear whether and how these beneficial symbionts are transmitted vertically from parent to offspring. Using comparative 16S rRNA amplicon sequencing and direct experiments with engineered bacteria, we provide evidence for vertical transmission of locust gut bacteria. The females may perform this activity by way of inoculation of the egg‐pod's foam plug, through which the larvae pass upon hatching. Furthermore, analysis of the composition of the foam revealed chitin to be its major component, along with immunity‐related proteins such as lysozyme, which could be responsible for the inhibition of some bacteria in the foam while allowing other, more beneficial, strains to proliferate. Our findings reveal a potential vector for the transgenerational transmission of symbionts in locusts, which contributes to the locust swarm's ability to invade and survive in new territories.