A strange thing happens when desert locusts get crowded together. They undergo a Jekyll and Hyde transformation.
In their solitary phase, locusts are unassuming insects. Their brown-green bodies are camouflaged to blend into the background and they walk slowly with a low, creeping gait. They generally avoid other locusts unless they are mating — or if they are forced together by food shortage. When this happens, the crowding of solitary locusts together induces a change. The insects transform into what’s known as their gregarious phase. Gregarious locusts are colorful, move faster, and are attracted to other locusts. It is in this phase that locusts form the oppressive swarms that can blacken the skies and decimate crops.
The solitary and gregarious phases differ in their looks, behavior, and life history, but do they also differ in their learning and memory capabilities? The learning and memory capabilities of animals are often adapted to their particular ecology and life history. This could be problematic, however, for an animal like the locust in which adults can transform from one phase to another; memories that are adaptive for a solitary lifestyle may not serve the insect in its gregarious way of life.
PatrÃcio SimÃµes, Jeremy Nivens, and Swidbert Ott decided to investigate how locusts learn and what they remember . They used an associative training technique: First, they paired an odor (like lemon or vanilla) with another stimulus (like food). Then they presented the learned odor and another odor at the two ends of a Y-shaped maze and recorded which arm of the maze the locust chose to walk down.
When an odor was paired with a food reward, all the locusts, regardless of phase, were able to learn the association. But the researchers found a difference between the phases when an odor was paired with a toxic food. Solitary locusts learned this association right away, avoiding the odor associated with the toxic food on the first test. Gregarious locusts did not avoid the odor until several hours later.
SimÃµes, Nivens, and Ott repeated the experiment with solitary locusts that had been crowded for 24 hours, and so were in the early stages of the gregarization process. These locusts were able to learn the positive association between an odor and food, but they showed no aversion to the odor paired with the toxic food at any time point tested. Their ability to form an aversive memory was blocked completely. And this failure in learning was specific to the aversive association, not reflective of a general impairment in learning.
The researchers hypothesize the delay in aversive learning in gregarious locusts is a consequence of the different ways in which the two phases form aversive memories. “We think that faster aversive learning is mediated by taste,” says Jeremy Niven. “The solitary locusts taste the bitter compound in the food and form an aversive memory. On the other hand, the gregarious locusts bypass the taste and only form aversive memories when they have ingested a toxic compound, and it’s this need to ingest the compound that causes the delay.”
This difference seems to relate to the different lifestyles of solitary and gregarious locusts. The solitary locusts dislike the taste of bitter compounds. The ability to quickly form aversive associations should help solitary locusts avoid ingesting toxins. But in their gregarious phase, locusts actually seek out some plants containing bitter compounds to make themselves distasteful to predators. In this case, the lack of a rapid, taste-mediated aversion to bitter compounds helps the gregarious locusts eat the bitter plants they need to defend themselves. Recently crowded locusts, the ones in the early stages of gregarization, seem to lack the ability to form aversive associations altogether. This allows them to eat greater amounts of bitter compounds without forming aversive memories.
A Plague of Learning Locusts
Finally, the researchers looked at how this might work with the real-world case of hyoscyamine (HSC), a toxic alkaloid found in some plants native to the locusts’ habitat. Solitary locusts avoid plants containing HSC, but gregarious locusts prefer them and seek them out. In tests, solitary locusts avoided an odor associated with HSC, whereas gregarious and recently crowded locusts tended to approach it.
This seems like it would pose a problem for a solitary locust that learns to associate an odor with food containing HSC but then undergoes gregarization. As a gregarious locust, it would need to seek out and eat plants containing HSC. What mechanism allows these locusts to start to eat the toxins they need?
SimÃµes, Nivens, and Ott took solitary locusts that learned an aversive association between HSC and an odor, crowded them to induce gregarization, and then exposed them to the odor-HSC pairing a second time. When tested in the Y-maze, these locusts no longer avoided the odor paired with HSC. This demonstrates that recently crowded locusts can update their memories upon re-exposure to the same stimulus. The experience of crowding alone transforms a further exposure to the odor-toxin pairing from an aversive experience to a positive experience that overrides their previously formed aversive memory. “This provides the means for the solitary locusts to switch their memories, helping them to adopt a new gregarious life history,” says Niven.
The crowded conditions that induce gregarization in locusts also produce an intense competition for food. Gregarious locusts eat all available plants in their path, but they preferentially eat plants with toxic compounds to become unpalatable to predators. Simple learning mechanisms, combined with hunger and competition for food, allow locusts undergoing gregarization to update and override previously formed aversive memories when they are re-exposed to the same stimuli. They effectively retrain themselves: locusts driven to hunger by overcrowding eat the plants containing HSC. But during gregarization, aversive memory formation is blocked. So they form a new, positive association with the odor they previously association with an aversive toxin.
“We think the mechanisms we’ve uncovered provide a means for the solitary locusts to be able to change phase and still behave appropriately,” Nivens says. They allow solitary locusts to make a complete transformation — in looks, behavior, and learning — to become part of a ravenous swarm.