Image Source: https://www.nature.com/
This year is a plague year. The COVID-19 pandemic, caused by the coronavirus SARS-CoV-2, is burning across the globe as we anxiously await an effective vaccine or drug to control it. Another plague, of a much older kind — one that is not curable with vaccines or medicine — is currently raging in Africa (Fig. 1) and the Middle East. Seasons of unusually heavy rains, driven by climate change (see go.nature.com/3fchnrm), have created population explosions of swarming desert locusts (Schistocerca gregaria). Swarms can contain billions of insects and cover hundreds of square kilometres. These insects strip vegetation and crops, threatening the precarious existence of subsistence farmers and contributing to food insecurity in vulnerable regions. The only effective weapon for fighting such locust plagues is the aerial spraying of pesticides, but the swarms are fast-moving and unpredictable, and spraying devastates beneficial insects.
How do these vast swarms of voracious insects form, and what can be done to stop them? Writing in Nature, Guo et al.1 identify a pheromone molecule of the migratory locust (Locusta migratoria) that might hold the key to swarming behaviour, and the authors’ discovery raises the possibility of using locusts’ own pheromone to combat this threat.
L. migratoria is a species of grasshopper that begins its life as a benign individual leading a solitary existence. But solitary locusts can attract each other to create ever-larger groups of gregarious locusts. During the process of joining a group, the pigmentation of solitary locusts changes from green to black, in an alteration regulated by a neuropeptide molecule2. The gregarious insects also begin to produce the molecule phenylacetonitrile, which is metabolized into cyanide and used as a type of chemical warfare against predators3.
Researchers have long assumed that an aggregation pheromone was the trigger for swarms, but no molecule had yet satisfied the conditions of being a candidate pheromone. For this, it would need to be a single type of molecule isolated from a natural source that, by itself, has the biological activity of interest — and that, when chemically synthesized in the laboratory, has the same activity as the biological substance4,5.
From a collection of 35 compounds emitted by locusts6, the authors identified 6 that are highly enriched in gregarious but not in solitary insects. Guo and colleagues tested each compound for its ability to entice locusts. Only the molecule 4-vinylanisole proved to be highly potent, and it attracted male and female locusts at both juvenile and adult developmental stages. Crucially, 4-vinylanisole was equally attractive to both solitary and gregarious locusts. This suggests that the ability to sense this proposed aggregation pheromone is innate.
The concentration of 4-vinylanisole in the air increased markedly when the population density of locusts rose. This is consistent with the molecule having a role in triggering the positive-feedback loop that gathers gregarious locusts as a swarm grows. The authors carried out a clever experiment to determine how many solitary locusts need to be crowded together to induce the production of this aggregation pheromone. The answer is remarkable: just four or five suffice.
How do locusts sense 4-vinylanisole? This molecule is a volatile odorant — classified as smelling sweet to humans — and the authors hypothesized that olfactory neurons in the insects’ antennae would detect it. Indeed, recordings from individual sensory hairs on an antenna allowed the authors to pinpoint one type that selectively responded to 4-vinylanisole. Consistent with the discovery that solitary locusts are as behaviourally sensitive to 4-vinylanisole as are gregarious locusts, the researchers found that the olfactory neurons of both types of locust were extremely sensitive to this pheromone.
The authors next set out to see whether they could identify an odorant receptor protein that could detect the molecule. They profiled 31 of the 141 known locust odorant receptors and identified a single one, called OR35, that was strongly and selectively activated by 4-vinylanisole. To prove that the Or35 gene encodes the receptor that mediates detection of this molecule, Guo and colleagues used the genome-editing technique CRISPR–Cas9 to generate mutant locusts that lacked this gene, and then tested the behavioural responses of the insects. These mutant locusts did not have antennal responses to 4-vinylanisole and were unable to detect the pheromone and respond behaviourally. This finding is exciting, because it indicates that a locust can be engineered to be immune to the effects of the pheromone. In principle, such an insect would not be expected to convert into the gregarious form.
In a final series of experiments, the authors put the aggregation pheromone to the test. In outdoor trap experiments on artificial turf, sticky traps baited with 4-vinylanisole were highly successful at trapping dozens of locusts released from the laboratory. Sticky traps of the same type, deployed in the field in a wetland reserve near Tianjin, China, successfully caught a modest number of wild locusts.
The first insect pheromone to be identified was bombykol, from the silkmoth Bombyx mori4. It took more than 55 years from the report of that discovery for scientists to reach the milestone of generating a mutant insect lacking the bombykol receptor7. New tools now enable much swifter progress. This research by Guo and colleagues covers remarkable ground in moving from the identification of the pheromone, to pinpointing the sensory neurons and odorant receptor that detect it, to generating a mutant insect that loses sensitivity to the pheromone, and to providing initial evidence that the molecule functions in the field to lure locusts.
Several important questions remain. It is not clear whether 4-vinylanisole is responsible solely for the initial aggregation of locusts, or whether it also triggers the pigmentation change and subsequent aggressive swarming behaviour seen after locusts gather. It is possible that the aggregation pheromone merely brings locusts together and that other, secondary mechanisms, and perhaps extra volatile signals, then induce further changes to the morphology and behaviour of the insect. Further investigation is needed to determine whether desert locusts also respond to 4-vinylanisole.
How might the production of 4-vinylanisole be triggered in a manner that is dependent on insect population density? One possibility is that locusts self-monitor their own production of the pheromone and that, as the density and concentration of the pheromone increase, the insects’ olfactory systems begin to adapt. This might lead to an upregulation of pheromone, similar to that seen in the Colorado potato beetle (Leptinotarsa decemlineata), which upregulates pheromone production when its antennae are removed8. The neural circuits that mediate this pheromone detection, production and pheromone-sensing behaviour in locusts remain completely uncharted.
Finally, how might this discovery be applied to the practical problem of locust plagues? The authors show that 4-vinylanisole can trap locusts. The efficiency was modest, however, and to scale up the trapping capacity, a more potent version of the pheromone would need to be developed, as well as more-powerful trapping technology. Most exciting is the possibility of using OR35 as a tool to identify compounds that block the activity of this receptor. The discovery of such a molecule might provide a chemical antidote to insect aggregation and cause locusts to ‘stand down’ and return to their peaceful, solitary way of life.
Story Source: https://www.nature.com/articles/d41586-020-02264-x