Silent Invasion: How Parasitic Queens Make Ants Kill Their Mother

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Worker ants normally protect their mother, maintain the nest, and care for the larvae. Yet in a single moment they can turn on their own queen, tear her apart, and eventually kill her. This gruesome matricide is set off by the clever manipulation of two species of parasitic ants, which ultimately take over the colony. 

The phenomenon was documented by ant enthusiasts and researchers at Kyushu University and offers a new perspective on the evolution of social parasitism in ants.

Ants form highly organized societies. Worker ants are daughters of the queen. They never reproduce and instead devote their entire lives to supporting the queen and the colony. The mother queen is the colony's lifeline, and under normal conditions the workers never attack her.

In this new study, two parasitic species in the genus Lasius were found to infiltrate colonies of other Lasius species. These invading queens use a parasitic strategy that forces the workers to kill their own queen by spraying a liquid believed to be formic acid.

Stealthy New Queens

The study focused on new queens of Lasius orientalis and Lasius umbratus, the latter often called the yellow shadow ant. Both species follow a life history known as temporary social parasitism. A newly mated queen does not build her own nest. Instead, she enters a host colony on her own, eliminates the resident queen, and forces the host workers to raise her eggs and larvae. 

In the observations, Lasius orientalis targeted the yellow meadow ant, while the yellow shadow ant targeted Lasius japonicus. All of these species belong to the genus Lasius, and these host relationships had been recorded before.

The phenomenon was first discovered by two ant enthusiasts. In 2021, Taku Shimada, who runs an ant specialty shop in Meguro, Tokyo, observed the behavior in Lasius orientalis and shared the findings on his blog and social media. 

In 2022, Yushi Tanaka from Hachioji, Tokyo, reported similar behavior in yellow shadow ants. Assistant Professor Keizo Takasuka of Kyushu University, who studies the ecology of parasitic wasps, contacted the two observers after 2022. Their collaboration led to the findings being compiled into a scientific paper. The results were published in November in the American journal Current Biology.

Infiltration

Before the parasitic queens were introduced into host colonies in the experiments, they were allowed to coexist briefly with the host workers and pupae. During this time they acquired the colony's scent, a scent-marking process that helps them avoid detection and aggressive attacks when they enter a new nest. Researchers believe the queens use a similar process in the wild.

Once a treated queen was placed in a host colony, she slipped in quietly and approached the resident queen without raising alarm. This was only the first stage of infiltration. The next step revealed the most significant discovery of the study.

The Critical Moment

The parasitic queen moved close to the host queen, arched her abdomen forward, and sprayed a liquid believed to be formic acid from her acidopore. In Lasius orientalis, up to fifteen sprays were recorded within twenty hours of the first one. In yellow shadow ants, two sprays were observed.

After the spray, the behavior of the surrounding workers changed dramatically. This is the core of the parasitic strategy. Workers would normally protect their queen and attack any intruding queen. Instead, once the spray was released, they turned on their own mother and began biting her.

The parasitic queen retreated immediately after spraying and took no part in the attack. The host queen was killed entirely by her own workers. With repeated sprays, the workers became increasingly aggressive, and the attacks eventually led to the queen being torn apart. The parasitic queen essentially tricked the workers into misidentifying their own mother as an enemy and drove them to commit matricide.

Taking Over

Matricide is rare in nature compared to infanticide, since it usually provides little benefit for the survival of the offspring. This newly reported behavior is a striking example of host manipulation. The researchers describe it as "matricide instigation."

Once the host queen has been killed, the colony is left with motherless workers. When the parasitic queen returns, the workers accept her as their new queen and begin to serve her, feeding her and raising her larvae.

This forms a temporary mixed colony that gradually shifts into a fully parasitic colony as the original host workers die out. This entire sequence of events defines the temporary social parasitism seen in Lasius orientalis and yellow shadow ants.

Social Parasitism

Although the two species belong to the same genus, previous studies suggest that temporary social parasitism evolved independently in each of them. This implies that spraying-induced matricide did not arise from a single evolutionary pathway. It may instead be an example of convergent evolution, in which different lineages develop similar traits on their own.

Known strategies used by parasitic queens to eliminate host queens include direct attacks such as decapitation. The newly observed behavior is an indirect method. This range of strategies offers new insight into the evolution of social parasitism. Many methods used by other temporary social parasites are still unknown, and more manipulation strategies like this one, or entirely different ones, may be uncovered in the future.

Deadly Spray

The sprayed liquid likely has two effects. It alters the host queen's chemical signals so she smells like a threat, and it disrupts the workers' perception in a way that triggers aggressive behavior.

Observations suggest the spray itself is not lethal. Instead, it causes the workers to mistake their own queen for an intruder. The chemical makeup of the spray is still unknown, and researchers have not yet identified the physiological pathways that lead to matricide.

This strategy of instigating matricide highlights a key idea in evolutionary biology. Takasuka and colleagues point to Richard Dawkins' concepts from The Selfish Gene and The Extended Phenotype, which describe how a gene's influence can reach beyond the body of the organism that carries it, shaping the behavior of other individuals or even altering the environment.

Ant Society's Cooperative Nature

In this case, the parasitic queen's genes lead to the spraying behavior that causes the host workers to kill their own queen. This ultimately allows the invader's genes to spread.

The highly cooperative nature of ant societies can be exploited in this way. Worker ants do not reproduce. From a genetic perspective, raising sisters, who share about three-quarters of their genes, is more efficient than raising their own offspring, which share half. This strong tendency to serve the colony can be manipulated by parasitic queens, who disrupt the colony's social structure with only a few drops of chemical liquid, without touching the host queen themselves.

Takasuka notes that although anthropomorphizing biological behavior is discouraged in evolutionary biology, imagining a queen being killed by her own daughters is unsettling. The strategy appears ruthless, yet it is not highly reliable and often fails. Only the parasitic queens that succeed are able to pass on their genes, highlighting the ingenuity and complexity of strategies that evolve in the competitive world of social insects.

Unlocking Hidden Worlds

This discovery was made through citizen science by two non-professional researchers. Taku Shimada, the first to observe the behavior, said, "I initially thought the parasitic queen would directly attack the host queen. But when I saw her spray formic acid and then watched the workers begin biting their own queen, I realized this was the real takeover method. I was thrilled and hope to see whether other species use the same strategy."

Takasuka added, "Even familiar species around us hold countless unknowns. Observing a single species over long periods without any guarantee of results is not easy. But careful, persistent observation can lead to new discoveries. The long hours of waiting and the unsuccessful attempts may be seen as a chance to glimpse a world no one has seen before."

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(Read the article in Japanese.)

Author: Yuki Kuroda, The Sankei Shimbun

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