How the iconic mass army ant raids evolved

Military ants form some of the largest insect societies on the planet. They are quite famous in popular culture, especially from a terrifying scene in Indiana Jones. But they are also important ecologically. They live in very large colonies and consume large amounts of arthropods. And because they eat so many other animals around them, they are nomadic and have to keep moving so they don’t run out of food. Due to their nomadic nature and massive food consumption, they have a huge impact on arthropod populations in tropical rainforest soils.

Their mass raids are considered the pinnacle of collective foraging behavior in the animal kingdom. Raids are a coordinated hunting swarm of thousands and, in some species, millions of ants. Ants spontaneously emerge from their nests, moving across the forest floor in columns to hunt for food. Raiding is one of the most emblematic collective behaviors of the animal kingdom. Scientists have studied their ecology and closely observed their complex behavior. And while we do know how these raids happen, we don’t know anything about their evolution.

A new study in Proceedings of the National Academy of Sciences led by Vikram Chandra, Postdoctoral Fellow, Harvard University, Asaf Gal, Postdoctoral Fellow, Rockefeller University, and Daniel JC Kronauer, Stanley S. and Sydney R. Shuman Associate Professor, Rockefeller University, combines phylogenetic reconstructions and computational behavioral analysis to show that the massive army ant raids evolved from a different form of coordinated hunting called group raids through the scale effects of increasing colony size.

Researchers have found that the ancestral state of army ant mass raids is the quite different group raids that their non-military ant relatives perform. The evolution of mass raids from group raids occurred tens of millions of years ago, and the transition from group raids to mass raids correlates perfectly with a massive increase in settlement size. .

“All of these ants are part of the Dorylinae subfamily,” Chandra said. “The first Colorado potato ants, which were not army ants, lived in small colonies of a few hundred workers. thousands – and often millions – of ants. “

Kronauer’s Social Evolution and Behavioral Lab at Rockefeller University studies the clonal raider ant Ooceraea biroi, a relative of army ants. Clonal plunderer ants are almost the only ant species that can be kept in a lab and experimented with indefinitely. They are also genetically treatable in that researchers can make mutants or transgenic lines to compare. But they are also poorly understood, little studied and difficult to find in the field. The mass army ant raid is well studied and described; however, the group raid is not. And understanding group raids is essential to understanding the evolutionary trajectory of mass raids.

“My goal has always been to study how social behavior evolves and is controlled, and how military ants evolved,” Kronauer said. “A few years ago, we discovered that the way clonal ants feed is through raids similar to army ant raids.”

To understand how the raids are structured and organized, the team collected a large number of video recordings of many settlements raiding under controlled conditions.

“Our goal was to understand what the underlying behavioral rules are followed by ants and how a raid emerges from the behavior of individual ants,” said Gal. “Tracking individuals in a dense colony is a challenge and does not have a generally applicable solution. This is especially true for small ants that like to form dense clusters such as thieving ants.

The researchers overcame this challenge by using custom computer vision software developed in the lab called anTraX which tracked and identified the ants based on small colored markings painted on their abdomen and chest. The method allowed them to collect precise trajectories for all the ants over several weeks with minimal human effort and without the need for expensive high-resolution cameras.

In a small nest of 25 ants, they used 5 sets of colors and painted each ant with a unique set of colors. The researchers placed a single fire ant nymph (the prey) in the foraging arena outside the nest. The nest sends a scout in search of food. Once the scout finds the food, she traces a pheromone trail back home. Inside the nest, she releases what researchers believe is a recruiting pheromone that attracts ants to her. They emerge from the nest and follow its trail to food during a group raid.

As researchers increased the size of the colony, so did the number of scouts sent to forage and they began to see more coordinated research activities. This same behavior is observed in army ants, but on a scale of tens of thousands or even millions of ants, with a very large increase in the number of scouts.

“Our behavioral analysis shows that group raids have a stereotypical structure, and that they are conserved across Dorylinae. Because the transition from group raids to mass raids during evolution is perfectly associated with massive increases in settlement size, we wondered if this had anything to do with it. with the transition in raid behavior, ”Chandra said. “We have gradually increased our colonies from 10 to 100 ants and we have seen this really nice increase in coordinated search behavior as you increase the size of the colony.

“Our experiments show that in larger colonies, ants are more synchronized in their exit from the nest to locate. In other words, when an ant leaves, the chances of more ants following it are higher in large colonies. While we cannot directly say much about the actual mechanism underlying this observation, we do know from other complex systems that an increase in synchronicity is the result of stronger positive reactions between individuals, ”said Gal. . “Within the army ants size limit, this will result in what we call a mass raid.”

But the resemblance to the behavior of army ants, given the increase in colony size, is not limited to time synchronization. Experiments have also shown that military ants and their relatives follow the same set of rules of behavior when foraging. A few military ants leave the nest early without a trace of pheromones outside. They exit hesitantly, then seem to wobble, turn around and run back. But there are ants inside the nest that want to leave, so they push them away, or they take their place. Because each ant that leaves and returns lays a trail of pheromones, the group slowly stretches the nest trail in gusts. This “push part” is how the army ants create a column of ants leaving the nest and traveling quite a distance. As the researchers expanded the colony size of the clonal raider ants, they observed the same behavior.

“It’s hard to see in the small settlements because there are so few ants,” Chandra said. “But we statistically show that this does happen and we have cases where it is quite dramatic. So even in small clonal ant colonies, each ant seems to follow very similar rules of search behavior as a army ant, although it might not look like it at first glance. And as you increase the size of the colony, the interactions between these ants lead to better coordination, you start to see “groups of” push “more obvious and you start to see spontaneous columns of ants leaving the nest.”

To test this twice, the team experimented with two colonies of 5,000 workers each, which is an order of magnitude larger than that seen in natural colonies of this species. In these studies, the raids showed the four hallmarks of massive army ant raids: a large number of ants participating in the raid, a branching path that allows the army ants to loot multiple sources of prey, recruitment that occurs outside the nest. on the raid front, and a spontaneously initiated raid.

At small colony sizes, these rules manifest as group raids, and as colony size increases – either experimentally or during evolution – these rules give rise to mass raids. The team concluded that the expansion in colony size among army ant ancestors was enough to have caused the transition from group raid to mass raid behavior.

“The most common pattern is probably that collective behavior evolves through natural selection acting and changing the rules of interaction followed by individual animals,” Kronauer said. “But our study is a good example of a different mechanism: the scale effects associated with group size can give you radically different results in terms of collective behavior, even if the individual rules don’t change much.”

Gal agreed: “Of course, it has long been known that changing the size of a group can have a dramatic effect on emerging collective behavior. This has been shown both theoretically and experimentally. We have now shown that this effect can also be exploited by evolution, and that collective behavior can be adapted over evolutionary time scales without actually changing the behavior of individuals. “

As far as is known, the coordinated behavior of clonal thieving ants is one of the most complex social behaviors that can be induced or studied in the laboratory. The authors are currently working on a detailed study of the behavior of individual ants during raid and how raid structure responds to variations in environment and colony composition.

“We suspect that ants specialize to some extent on specific tasks,” Chandra said. “There is probably a very interesting division of labor going on, and there is also clearly complex communication – the ants use several different pheromones to talk to each other and organize the raid. And there are several decisions the colony has to make in the process. It’s incredibly rich behavior and there are a lot of questions we might ask ourselves in the future and we’re setting the stage for that. ”


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