Some fungi, viruses and bacteria have evolved a spine-chilling way of being transmitted from one host to another. They turn their hosts into witless zombies

The zombies we know from fiction are ferocious, flesh-eating post-humans. And while such stories have never come true, nature is full of disturbingly similar cases of zombification among plants and animals. Sometimes the parallels are striking.

There is something particularly disconcerting about the idea that an animal's behaviour could be drastically changed by an infection or parasite, but it is a phenomenon well-established in nature.

In fact, fossils showing evidence of zombie ants – including the apparent marks their infected, mind-controlled bodies left on leaves – have been found dating back 48 million years.

Meet the real-life zombies, some of which are even stranger than fiction.

Zombie ants

A couple of years ago, Matt Fisher was on a night-time research stroll through the dense forests of French Guyana when he stumbled on a grisly sight. "We found the cadavers of insects that were parasitised, clamped up high to vegetation, with these horrendous spore-bearing bodies projecting out of their skulls," he recalls.

Fisher, a fungal disease epidemiologist at Imperial College London, knew instantly what they were. These were the remains of "zombie" ants – insects infected with a fungal parasite that controls their body and mind, making them crawl up plants where they stay put. When they die, their infectious fungal spores rain down on other ants below, spreading the contagion far and wide.

While the zombies of fiction often spread the infection through a nasty bite, these ants fix themselves to plants in a similar way. Sometimes, they grip on with their jaws in a death lock. They then die with that horrifying clench intact.

Once infected, the zombie ant will mindlessly crawl to a specific type of location

The group of fungi that can do this belong to the genus Ophiocordyceps. Once infected, the zombie ant will mindlessly crawl to a specific type of location determined by the species of fungus to which it has fallen victim.

Perhaps the most famous fungus, Ophiocordyceps unilateralis, prompts its hosts to end their days perched under a leaf. Those that have succumbed to Ophiocordyceps australis, meanwhile, will die in the forest litter below.

It is not immediately apparent how a fungus has this surprisingly specific effect on an organism so much more complex than itself. But David Hughes, Harry Evans and colleagues hope to find out – they have been studying cordyceps fungi for decades. Over the years, they have discovered that different species of Ophiocordyceps unilateralis have evolved to match the different lifecycles of whichever species of host ant they take as their victim. It is "a stunning example of coevolution", says Evans.

In a 2016 article, Evans and his co-authors explained that the fungus likely uses a series of enzymes that alter processes in the ant host's body. These enzymes may, for example, change the expression of genes in such a way that influences the ant's behaviour.

It is also known that, once "zombified", muscular tissue in the ants gradually breaks down.

There may also be direct manipulation of the ant's nervous system, and control of neurotransmitters or "chemical messengers" like dopamine – which can also modify behaviour. However, this interaction is not fully understood. What is clear is that more examples of fungi-insect zombies are still being discovered.

"The next question we are trying to solve is: does the same thing happen in spiders," says Evans. "And, the answer would appear to be: yes it does."

These real-life zombies now even influence the representation of zombies in stories. As they have become better known, cordyceps fungi have inspired modern tales about the undead. For instance, in M R Carey's novel, The Girl With All the Gifts, and in the video game The Last of Us, human victims fall foul of a fungal parasite, not a zombie virus.

Zombie parasites

The situation in which the lives of two organisms are directly linked – such as with a parasite and host – is known as symbiosis. In the insect world, there are lots of examples of this.

Take, for instance, the parasitoid wasp Glyptapanteles, which lays its eggs in the body of caterpillars. When the eggs hatch, the wasp larvae feed on the host caterpillar's bodily fluids before eating their way out and forming a cocoon nearby.

But the caterpillar, though damaged by this process, is still alive and remains in position as a sort of zombie bouncer that aggressively knocks away beetles that come near to – and might prey on – the cocoons. Researchers studying this have found that, with a zombie caterpillar guard in place, the number of predators approaching the cocoons can be halved – an obvious advantage for survival.

The term parasitoid means a parasite that eventually kills its host. There are plentiful examples of parasitoid wasps that influence host behaviour in gruesome ways.

Kelly Weinersmith, an ecologist at Rice University, studied one macabre example in early 2017. It has become known as the crypt-keeper wasp, or Euderus set.

The hole is smaller than usual and instead of getting out, its head gets stuck and it dies

This parasitoid wasp waits for other wasp species to make a gall: a growth on a plant when a certain wasp species lays its eggs.

The discovery was made after Weinersmith's colleague Scott Egan discovered an unusual wasp gall while out walking on a family holiday. In this case, the gall was created by a wasp species called Basettia pallida.

Usually, B. pallida will hatch and eventually make a hole in the gall before flying away. But with the crypt-keeper wasp at large, its fate is not so lucky. That is because Euderus set has arrived and laid its egg inside the gall or crypt.

 

"We don't know the mechanisms by which it does this, but it gets the first wasp that was in there to create an emergent hole," says Weinersmith. "But the hole is smaller than usual and instead of getting out, its head gets stuck and it dies stuck in that hole."

The crypt-keeper wasp is now in charge. It eats the trapped, dead wasp for sustenance as it grows. "When it's done developing, it emerges through the head of its host," says Weinersmith.

So parasite begets parasite. The first wasp, B. pallida, itself a parasite of the tree, has been turned into a sort of suicidal zombie – and nutritious fodder for its own parasite, the crypt-keeper. The two individual cases of control here, one dependent on the other, makes this is a rare example of hyper-manipulation, Weinersmith says.

Sex zombies

If a zombie is an organism whose behaviour has been drastically modified in order to benefit its parasite, then another bizarre example can be found in the Japanese tree frogs of South Korea. In March 2016, Bruce Waldman at Seoul National University and his student, Deuknam An, published evidence for an extraordinary behavioural manipulation caused by a pathogenic fungus, Batrachochytrium dendrobatidis.

The fungus is a well-known threat to many frog species, but Japanese tree frogs in Asia do not seem to be dying off so suddenly when a population is infected. When Waldman and An listened to the mating calls of 42 male tree frogs, they realised that the nine that were infected with Batrachochytrium dendrobatidis had calls that were faster and longer – making them more attractive to potential mates.

Since the paper was published, Waldman and his team have recorded the calls of healthy frogs in the field before collecting them for study in the lab. The frogs' calls were recorded again after the animals had been infected with the fungus.

The amphibians may essentially have been turned into "sex zombies"

With another group of frogs, calls were recorded after their fungal infection was treated. In both groups, the calls changed as a direct result of the infection, the team proposes.

"Still, we cannot say for sure whether the call differences are attributable to the fungus manipulating the host," Waldman says. It could, for example, be due to some other reaction that the frogs are having to their infection.

Matt Fisher says the amphibians may essentially have been turned into "sex zombies", whose subsequent interactions with mates only increase the likelihood of the fungus spreading further. "It's not a proven hypothesis by any means, but the data is fairly strong," he says.

Mutant zombie plants

Perhaps one of the most surprising examples of a real-life zombie in nature is not in animals whose behaviour goes awry – but in plants that are transformed into mutant versions of themselves.

Saskia Hogenhout at the John Innes Centre and colleagues discovered the mechanism by which one group of bacteria, phytoplasma, transform helpless plants into zombies. They published their research in 2014.

The bacteria in question need to be spread by insects that feed on plant sap, for example leafhoppers. But in order to attract these vehicles of contagion, infected plants must first be bent to the bacteria's will.

"It looks like the parasites are taking over the plants," says Hogenhout.

The parasite is interfering with some very basic plant processes and changing the identity of the plants

Hogenhout and her team discovered that the bacteria were secreting proteins that change molecular processes inside the plants. That is, they alter transcription factors: the plant's own proteins that control gene expression and help differentiate different parts of the organism, for example a leaf versus a flower versus a stem.

The bacteria's invasive proteins displace the plant's own ones to the extent that the infected plant begins to transform itself. Flowers on the plant begin to morph into green flowers, essentially becoming leaves. The infection makes them more attractive to the insects that will pick up the bacteria and carry them to new plant hosts.

"It was very clear that the parasite is interfering with some very basic plant processes and changing the identity of the plants, and that's what zombies are really," says Hogenhout. "They're taking on a different identity."

The zombie plants are a particularly interesting example because the plant itself does not ultimately die as a result of the infection. It has simply been transformed into a useful vehicle for furthering contagion. As biologist Jon Dinman at the University of Maryland points out, some successful "zombie"-style infections keep the host alive.

In general, disease is most likely to transmit between organisms when its virulence – its ability to harm them – is kept in check. This is exactly what happens with the zombie plants, for instance.

Fortunately humans are not existentially threatened by these pathogens.

The same cannot be said for many insects and other organisms, however. In forests all over the world, zombie hosts are already out there, their minds and bodies twisted under the spell of spectacular parasites.

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