Alberta researchers investigate how zombie parasites take control of ant brains

In the southeast corner of Alberta, the Cypress Hills are a dramatic sight rising out of a sea of prairie.

Look down, and you’ll see another drama playing out. 

Ants are clasped onto plants and shrubs throughout the Cypress Hills Provincial Park against their will, waiting to be accidentally swallowed up by an unsuspecting herbivore. 

The culprit is the parasite Dicrocoelium dendriticum, a worm with an incredible ability to zombify its host.

According to researchers at the University of Calgary and University of Lethbridge, this parasite sits alone in the hall of fame of parasite manipulations because it is able to turn its control on and off — something not seen elsewhere in the world of zombies. 

Zombies are everywhere

Zombie parasites are quite common in nature, says Cameron Goater, a parasitologist and professor emeritus at the University of Lethbridge. 

“Almost every taxon [species] of hosts on the tree of life contains parasites or are infected with parasites that lead to manipulation,” said Goater. 

The goal is often to get from one host to the next. Take the famous Cordyceps fungus popularized in the video game franchise turned hit HBO show The Last of Us. Infected ants climb plants and die so that the fungus can burst out and rain spores down on unsuspecting ants. 

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Or the horsehair worm that drives crickets to commit suicide by jumping into water so the worms can emerge and mate. 

These examples and nearly all others in the animal kingdom end in the host's death, but Dicrocoelium is different because the nature of its life cycle incentivizes keeping the host alive. 

Dicrocoelium has what parasitologists call a complex life cycle involving multiple hosts. The final host is a grazing mammal like elk, deer or cattle. Adult worms live in their livers, and their eggs are pooped out and eaten by snails. 

In snails, the egg divides into hundreds of larval forms called cercaria. These are packaged in mucus and coughed out as a slime ball. (That is the official term.) Slime balls are then eaten by ants, and all but one cercaria go to the abdomen, while a single "brainworm" cozies up next to the ant's brain. 

This is where the challenge begins. 

“The problem is the final host almost never ingests ants,” said Goater. “In many cases, things like deer and elk and cattle actually avoid ants.” 

So, it helps to have a brainworm that compels the ants to climb plants where they can be accidentally eaten.

But this solution is risky. Ants clinging to vegetation are exposed to predators, they can’t eat and, importantly, they are extremely susceptible to dehydration.

“The solution to that problem is to detach from a plant and go back to the nest,” said Goater. “That's where this on-off switch comes from.”

For the rest of their lives, these ants climb plants and cling on so long as the temperature is below approximately 19 C. 

How can a parasite inside an ant know what temperature it is outside and adjust its mind control in response?

“That's exactly the kind of question that keeps us awake at night,” said Goater, “because it seems that the mechanisms that run that might be something completely new.”

How to take over a mind

The first step to understanding this phenomenon is to look at the genes being expressed during and after the clinging behaviour, and comparing this with uninfected ants.  

“We've gone inside the brain of the ant to try and determine what those changes are from the ant perspective,” said James Wasmuth, a parasitologist at the University of Calgary. “And we see a lot of changes in different biochemical pathways when it's doing the zombie behaviour.”

While it appears the ant is not sensing the environment in a normal way when it’s under parasite control, it is difficult to pinpoint one change that is driving behaviour, said Wasmuth.

According to Shelley Adamo, an insect neurobiologist and professor emeritus at Dalhousie University, this is to be expected. 

“When I first got into this business, the assumption everyone had was there was a magic bullet,” said Adamo.

However, the more scientists learn about these systems, they realize that’s not the case.

“Evolution rarely does the grand redo,” Adamo said. 

Parasites like Dicrocoelium work by tapping into existing systems, which are themselves extremely complex. 

“We rely on chemicals for communication from one nerve cell to another; it's not hardwired,” Adamo said.

This gives the parasite ample opportunity to interfere, gradually evolving ways to nudge these systems to their benefit. The result is a plethora of subtle changes culminating in the precise manipulation.  

Solving that puzzle requires many careful experiments where some genes are suppressed or not to see if the manipulation remains. 

However, Adamo is excited by the first steps taken by the Alberta researchers toward identifying potential molecules involved like adenosine. 

"That molecule is interesting because it's also involved in immune systems as well as neural systems," said Adamo.

According to Wasmuth, adenosine regulates stress and feeding, as well as sleep. 

“A massive increase in adenosine pathways induces sleep in other animals. So, we think that the worm is somehow controlling the invertebrate sleeping,” said Wasmuth, “but we don’t actually know.”

Along with adenosine, certain biochemical pathways related to smell, metabolism and circadian rhythms appear to be altered, Wasmuth said.

No magic bullet but lots to learn

Understanding how a parasite changes behaviour means deciphering the chemical code behind the behaviour. 

“These parasites have tapped into a really vital clue about how brains work because they can subtly alter something that causes a behavioural shift which is quite dramatic,” said Adamo. 

Humans are equally susceptible, says Adamo.

“If you take drugs, for example, you can alter the way your brain perceives things."

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This is the gift and curse of animal brains: they are extremely plastic and can learn throughout their lives, “but the weak side is that you are also open to manipulation if somebody knows the chemical code,” said Adamo.

Why Cypress Hills?

Goater believes Dicrocoelium can teach us about the consequences of humans manipulating nature. 

This parasite was introduced to Canada likely from importing sheep and other animals from Europe decades ago, says Goater.

So why don’t we see it nationwide? 

“This is what we call an anthropogenic introduction of a parasite or disease, because humans brought it in, and almost certainly the way we manage the landscape influences transmission as well,” Goater said. 

“We do a lot of things in that park that really benefit transmission, and one of them is we control fires and that leads to high snail densities, high ant densities,” Goater said. The park is also managed for cattle grazing, which likely contributes as well. 

Humans may have inadvertently created the perfect conditions for this parasite in Alberta, which according to Goater is pretty amazing given its complex life cycle. 

“When it moved over and colonized these unique areas, it had to jump into a new species of snail, into a new species of ant and then to a new species of grazer,” he said. 

Understanding the conditions that allowed all those factors to line up, said Goater, can inform how we deal with all sorts of emerging diseases.