Scientists document a new form of host manipulation where an invading, parasitic ant queen "tricks" ant workers into killing their queen mother. The invading ant integrates herself into the nest by pretending to be a member of the colony, then sprays the host queen with fluid that causes her daughters to turn against her. The parasitic queen then usurps the throne, having the workers serve her instead as the new queen regent. This work appears in the Cell Press journal Current Biology on November 17.
"At first, I wanted the title of this study to exemplify a fable where a daughter is tricked to kill their mother. I asked CHATGPT if this kind of matricide appears in a fictional story, but it said no such story exists," says lead author Keizo Takasuka of Kyushu University. "So, this is an example of nature going beyond what we've seen in fiction."
Matricide, a behavior where offspring kill or eat their mother, is a rarely seen phenomenon in nature. Despite appearing maladaptive at first glance, it does offer advantages by either nourishing the young and giving the mother indirect benefits through increased offspring survival or allowing the young to invest in offspring of their own. "Up until now, only two types of matricide have been recorded in which either the mother or offspring benefit. In this novel matricide that we reported, neither profit; only the parasitic third party," says Takasuka.
The ants Lasius orientalis and umbratus, commonly referred to as the "bad-smell ants" in Japanese, are so-called "social parasites" that execute a covert operation to infiltrate and eventually take over the colony of their unsuspecting ant queen hosts, Lasius flavus and japonicus, respectively. The parasitic queen takes advantage of ants' reliance on smell to identify both friends and foes to dupe unsuspecting worker ants into believing she is part of the family.
"Ants live in the world of odors," says Takasuka. "Before infiltrating the nest, the parasitic queen stealthily acquires the colony's odor on her body from workers walking outside so that she is not recognized as the enemy."
Ant species taking over another's colony using scent as cover is not a new phenomenon; there are many examples of ant social parasitism where, after entering a colony, a parasitic queen will directly kill the colony's queen and convince the workers to serve her instead. There have even been prior reports of workers killing their queen in response to a social parasite's presence, but only now have the actions that cause this matricidal behavior been observed.
Once these "bad-smell" ants have been accepted by the colony's workers and locate the queen, the parasitic ant douses her with a foul-smelling chemical researchers presume to be formic acid—a chemical unique to some ants and stored in a specialized organ. "The parasitic ants exploit that ability to recognize odors, we believe, by spraying formic acid to disguise the queen's normal scent with a repugnant one. This causes the daughters, who normally protected their queen mother, to attack her as an enemy," Takasuka says.
Then, like fleeing the scene of the crime, the parasitic queen immediately (but temporarily) retreats. "She knows the odor of formic acid is very dangerous, because if host workers perceive the odor they would immediately attack her as well."
She will periodically return and spray the queen multiple times until the workers have killed and disposed of their mother queen. Then, once the dust has settled, the parasitic ant queen returns and begins laying eggs of her own. With this newly accepted parasitic queen in the colony and no other queen to compete with, the matricidal workers begin taking care of her and her offspring instead.
Now that this kind of behavior has been captured on video, Takasuka and his research team will explore how far this unique form of matricide extends, and whether it can be found in other insects outside of ants. "Only ants in the subfamily Formicinae use formic acid to elicit violent responses, but I don't rule out the possibility that non-formic-acidic ants and social wasps commit matricide in similar ways," Takasuka says.