Natasha Mitchell: All in the Mind -- beware the parasites have arrived and they're ready to take over your brain!

Film Trailer: Parasite: Be assured, Parasite is the most gripping and frightening movie you will ever see. You are about to witness the future, be warned it is a shocking sight.

David Hughes: We just don't like the idea of something else or somebody else or anything else taking over our behaviour, we think that's very special to us.

Natasha Mitchell: Well it spooks us doesn't it?

David Hughes: Yes, absolutely and if you can take a step back and just think about the incidence of parasites, half of life on the planet is a parasite and many of those have evolved very cool tricks either to take over behaviour or even just take away food from us during the infection process.

Kevin Lafferty: Parasites are trying to get on with their lives, just like us but they're trapped within our bodies and so one of the ways that they've been able to figure out to be more efficient at the things they do is just to have us do some of their business for them. Probably I think one of the most dramatic ones is a worm that lives inside crickets.

David Hughes: Fred Palmers in Montpellier in France had gone all the way from New Zealand to study this and then a lady, a private person in France, had realised that these crickets were jumping into her swimming pool every night.

Kevin Lafferty: And this worm needs to go to a stream where all the other worms in the worm population will get together and form a huge ball and have this sort of mating orgy that lasts for weeks in the stream.

But get to the stream they have to trick the cricket into jumping into the stream and crickets don't normally do that.

David Hughes: So he quickly went back to France and discovered what happens in this case is that the crickets come out of the woods and jump into swimming pools at night time between 10 o'clock and 2 o'clock in the morning.

Kevin Lafferty: So the worm eats the cricket inside out, eats all the fat and all the stuff that isn't tied to the musculature and then it makes the cricket incredibly thirsty and then the cricket goes on essentially this quest for water and jumps into the stream and as it does that the worm pops out of the anus and it's about a foot long worm that pops out of a two inch cricket.

Natasha Mitchell: That is incredible.

Kevin Lafferty: So that's a powerful manipulation of behaviour, clearly countered to those interests. I don't know the whole thing is both fascinating and creepy at the same time.

Natasha Mitchell: It sure is, we have ways of making you think. Prepare yourself for a creepy encounter with suicidal crickets, mad rats and zombie ants. Parasites have developed uncanny ways of co-opting brains to get what they want. One of my guests even argues they could be changing the personality of whole human civilisations.

Hi, Natasha Mitchell with you and if you heard The Science Show with the RadioLab on parasites earlier this year here's another opportunity to be parasitised.

Film Trailer: Parasite: It's the most terrifying form of fear. Parasite. That thing on your stomach ... The new strain of parasite when it reproduces it will cast millions of microscopic spores into the air ... Just move your legs towards me, real slow, real slow.]

Natasha Mitchell: No it's not a monster movie parasites are as much a part of the symbiotic way of the world as we are. We cohabit, they inhabit -- and sometimes us. The parasitic mission of course is to live and sexually reproduce. And often that involves the manipulation of the behaviour of their hosts.

Take Toxoplasma Gondii: if you're pregnant you've probably been tested for this parasite because it can cause brain damage and blindness in your developing foetus. So it's definitely one to know about. Most of us though don't know. In fact you might have it, I might have it, even ecologist Dr Kevin Lafferty from the United States Geological Survey could too.

Kevin Lafferty: Well I actually do know that I don't have it...

Natasha Mitchell: Have you got it?

Kevin Lafferty: But you don't know if you have it or not. Chances are reasonable that you do; somewhere between a third to a half of the world population is infected with this parasite. Toxoplasma is a parasite of cats. That's where this protozoan has sex. And to get back to a cat it has another one of these predator-prey transmitted life cycles. Basically cat faeces go out in the environment and they contaminate the soil. Things like mice or birds or whatever contacts that soil and can become infected and then a cat can come along and eat an infected mouse and that's how the lifecycle is completed.

Humans are commonly exposed to toxoplasma either by contact with contaminated soil or by eating undercooked meat products.

Natasha Mitchell: There was a 2002 figure that said that 38% of UK meat products being sold had toxoplasma gondii on it, that's kind of confronting isn't it?

Kevin Lafferty: Yeah, I guess what it says is only eat two thirds of UK meat products -- if you only knew which ones were which.

Natasha Mitchell: Dodgy stats -- anyway, go on.

Kevin Lafferty: I became interested in toxoplasma because I'd read some papers of folks that had studied the effect of the parasite on mice. So the parasite goes into many different types of tissues but it prefers to go into the brain of the intermediate host. What these researchers had done was some very sophisticated studies showing that infected mice lost their fear of cats. Specifically their fear of the smell of cat urine. But they also had increased activity, and the great thing about this experiment was that they were able to change the behaviour of infected mice back to normal by giving them a drug that killed the parasite. They could also do the same thing by giving them a mood stabiliser drug.

Here we have I think a really strong experiment evidence that parasites that are in the brain can manipulate behaviour in ways that make -- at least in this case it seems really obvious that this should make a mouse more likely to be eaten by a cat. But what fascinated me was that here we have a parasite that can do these amazing things in a mouse but when it gets into our brain it doesn't know that it's not in a mouse and it's trying the same tricks and the trick we think happens in the mouse is that it manipulates dopamine and perhaps some other things. And the way it does this is by continually provoking the immune system. It causes inflammation and that alters these neural modulators in our brain.

Natasha Mitchell: And if the Toxoplasma parasite is so common in humans then could it be infecting the personality of whole populations? Parasitologist Kevin Lafferty has a provocative hypothesis there -- wait for that in a moment. But let's hear another real life fable of parasite psychology first. The story of a fish, a snail and a bird.

Kevin Lafferty: We have these parasites called trematodes; they have very complicated life cycles: they live as adults in birds, in the gut of the bird and their eggs pass out with the bird's faeces on to the mudflats of an estuary. At that point a snail contacts the eggs and becomes infected. The worm grows up inside of the snail, it actually castrates the snail for life and then every afternoon the snail will shed these free-swimming stages that go out into the water and seek a fish. The stages that leave the snail look like little tadpoles but they're microscopic. They find the fish; they penetrate through the tissues and then form a cyst. They are essentially waiting for the bird to come along and eat the fish, that's how the life cycle is then completed.

Natasha Mitchell: Now what's interesting about this is that the fish's behaviour is changed reasonably markedly by the parasite. How? And then we'll discuss why.

Kevin Lafferty: We were really suspicious about the fact that these cysts were on the surface of the brain. What the parasite is looking forward to is the day that bird comes and eats this fish and it gave us the hypothesis that the parasite might be able to manipulate the behaviour of the fish in some way. And what we found was that infected fish had four times higher frequency of what we called conspicuous behaviours compared to uninfected fish.

Natasha Mitchell: So it was coming to the surface more or something like that?

Kevin Lafferty: They would do two things, they would come to the surface more frequently, and the other thing they did is they would roll over on their sides and when that happens in the field you see this bright flash, and that really attracted our attention and the idea was then to see whether or not that attracted the attention of birds, so we set up a field experiment. We made some large pens, we put fishes inside some were infected and some were not infected, and then we covered one of the pens with a netting to keep birds out. And the birds came, these are herons and egrets and they came and fed on the fish in our enclosures and they only took the infected fish.

You were ten to thirty times more likely to be eaten if you were infected. So that was a very clear demonstration that this parasite that lived on the brain by manipulating the conspicuous behaviours of these fish was able essentially to determine who lived and who died in the fish population in a way that helped it complete its own life cycle.

Natasha Mitchell: Because it ultimately wants to get back inside a bird and it's the only place it sexually reproduces. Did you work out a sort of mechanism for how it was changing the behaviour by infecting the brain in a particular way?

Kevin Lafferty: I have a student, Jenny Shaw, who's just finished her PhD and what she did was to grind up fish brains and she found that the more parasites that were in the brain, she got a big change in serotonin levels which is a neuro modulator. In her trials she took fish and she stressed them out, she chased them around the tank with a net, and that changes the brain chemistry of the fish in a way that -- essentially the characteristic of a stressed-out fish who is trying to escape.

But the infected fish didn't seem very stressed out. What the parasite appeared to do was to just make the fish less stressed when it was being chased around the tank.

Natasha Mitchell: So it bumped up the fishes' levels of serotonin in some way which diminished the fishes' anxiety and response to stressful situations -- a bit like antidepressants do.

Kevin Lafferty: Yeah, quite a lot like a living antidepressant.

Natasha Mitchell: Is there a risk that we anthropomorphise parasites and how they affect the behaviour of their hosts? We sort of develop a grand theory, a grand thesis about what are parasites capable of. Is there a risk of anthropomorphising?

David Hughes: I think there definitely is this risk and I think we do that with many biological subjects and also in the choice of the biological subjects we make as professional scientists. We tend to gravitate towards whatever resonates with us and definitely in the case of these zombie ants we do think about it in zombie behaviour yes.

Natasha Mitchell: Wait did ecologist David Hughes just say zombie ants? You'd better believe it.

[Ant sounds]
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An incredible recording made on an ant mound in British Columbia, Canada, by composer and media artist Matt Rogalsky.

Associate Professor David Hughes is on a worldwide quest for zombie ants and the fungus that's taken over their brains. And a recent fossil discovery suggests it's a parasitic relationship that may have been around for more than 48 million years.

David Hughes: Well we've already been three times to Brazil and also sampling in North America and South Carolina and now we're in Australia, we're going to be sampling in Cairns over a week also with a chap from the Brisbane Herbaria collection there. Definitely the Amazon is going to be a place we're going to, Ecuador and the Brazilian side and we're interested in the Honduras, Malaysia and Sri Lanka. Basically as many places as we can.

Natasha Mitchell: You're in search of one of the most dramatic examples of how a parasite can manipulate the behaviour of its host, and in this case the host is a humble ant. But what the fungus manages to achieve is really far from humble isn't it?

David Hughes: Absolutely, as with many examples of insects and fungi which infect them, it starts with a spore going through the insect's skin and then into the body of the insect and then the fungus and reproduces inside the body. In most cases then the fungus just kills the insect but in the case of these ants what happens is that the fungus produces a cocktail of chemicals, we don't know what they are at the moment, but they cause the individual ant to leave the nest, usually these nests are in the canopies of tropical forests, and the ants go down to the understory vegetation, they kind of walk around drunkenly for a while. After about two hours then they very precisely bite onto the underside of a leaf, not just any old leaf but leaves within a narrow range of the forest floor in a particular orientation and then they bite into the surface of the leaf -- not just any part of the leaf but into the main vein and then the ant is firmly attached upside down, attached to the main vein of the leaf and then it dies.

And all of this complicated behaviour is because the fungus is effectively choosing a nice place for it to grow once it kills the ant, because then it's going to use all the ant muscles and resources to produce fungal spores. And over the next coming days the fungus grows from being inside the ant to the outside effectively stitching the ant to the leaf and the fungus then reproduces.

Natasha Mitchell: And that's one dead ant, dead ant, dead ant. David is talking about a fungus called Ophiocordyceps, and carpenter ants, which nest in the canopy of tropical forests like those in Southern Thailand where he's done much field work, 300 km north of the Malaysian border.

David Hughes: So we actually mapped out 1,360 square metres of forest and looked under every single leaf and those ants are found under those leaves and just in order to get a really good map of the situation.

Natasha Mitchell: The ant is prompted by the parasite you think to come to a very particular level and you've actually investigated this, and it's a level that's ideal for the parasite to reproduce isn't it?

David Hughes: Yes, we've actually taken these ants from this particular level and put them back up into the canopy when they have been killed by the fungus or we put them down on the ground level, and the fungus is not able to reproduce or even to grow at ground level or in the canopy. The canopy is very dry and it's very hot and the ground is excessively wet and it's got a lot of movement, so the fungus is not able to live on the ground or in the canopy, it lives under the leaves at this particular height.

Natasha Mitchell: Amazing, so the ant comes down to a very particular height, they bite on to a leaf, you describe that as a death grip. At this point I gather the fungus really goes to town on the ant doesn't it so what have you observed there?

David Hughes: Absolutely, so very quickly after dying the fungus then changes its whole strategy from growing inside the ant in a particular single-cell stage to burst out of the ant's cuticle, growing sometimes onto the leaf to keep the ant attached to the leaf and then growing this enormous stalk out of the back of the ant's head. And from this stalk spores are produced which are then shot out to infect new ants.

Natasha Mitchell: This stalk is quite bizarre, I've seen the photos that you have of this, it's like a sort of extra limb that grows out of the ant's head at some point with a big circle of spores on the top.

David Hughes: Yes exactly, it's a really interesting feature of this group of fungi.

Natasha Mitchell: Just absolutely bizarre. Do we know how the parasite actually works inside the tiny nervous system of the ant -- because you've actually done dissections haven't you of ants to see where and how it's co-opting the anatomy of the ant?

David Hughes: Yes, so we've done dissections and we've actually with histological measurements we can see whereabouts the fungus are inside the body. We found they're not actually inside the brain, we find they are just dispersed inside the head region or inside other parts of the body. So we think that are not physically activating any part of the brain but producing chemicals that would then interact with the brain.

Natasha Mitchell: And so the ant dies and it has become a zombie, effectively, co-ordinated by a parasite fungus, so its body is there simply to serve the fungus?

David Hughes: Absolutely yes and then very quickly the fungus takes over and converts ant muscles into fungal tissue and at the same time the fungus has to deal with a whole range of different organisms in the forest which would be just as happy to eat the dead ant as the fungus is. And so it has to produce lots of antibodies which stop a lot of organisms taking over the ant.



Natasha Mitchell: It's intriguing isn't it?

David Hughes: And this is the reason why we're very interested in this group of fungi so one which infects caterpillars in the Tibetan alps has been used in human medicine for about 1,500 years, and in Chinese medicine particularly, and also in Western medicine. And we know that it has anti-cancer and anti-malaria and anti-TB properties. Because if its rarity it has been over-collected extensively, it's shot up to about $90,000 US per kilo.

Natasha Mitchell: Well that's a concern isn't it, the impact of deforestation must be enormous on this symbiotic story of parasite and host?

David Hughes: Yes it is, and there are some healthy signs about deforestation particularly in Brazil which has eased up on these things. So now that provides the impetus for us to go and discover some of these interesting metabolites in forests.

Natasha Mitchell: Incredibly, David with scientists at the Smithsonian have just reported on what they're confident is a 48-million-year-old fossilised leaf with those very characteristic bite marks of a parasitised ant, not just any hungry insect they think. The first evidence of behaviour modification by a parasite in the fossil record, 48 million years, that's one long and deathly love affair between a fungus and its ant isn't it?

I've popped the audio about that on my All in the Mind blog. and Associate Professor David Hughes there, about to take up a new position at Penn State University.

And on ABC Radio National's All in the Mind I'm Natasha Mitchell, it's parasites on the brain, on air and online at abc.net.au/rn/allinthemind.

Now if you're infected with rabies people are likely to know, the frothing at the mouth perhaps. But could another brain parasite be shaping the personality of our entire population? Entire civilisations even, without us knowing, and might we be less neurotic without it?

Recent research suggests that high infectious disease rates and lower average IQ could be linked -- with the message that keeping kids parasite free is as important as schooling. But take toxoplasma, that parasite we heard about earlier. Dr Kevin Lafferty has crunched some interesting data there.

Kevin Lafferty: The thing that interested me was we had these ingredients for an interesting story potentially. Firstly a parasite that manipulates behaviour in humans, secondly a very, very common parasite where maybe half of us are infected and thirdly a parasite that varies tremendously in its abundance from country to country.

What those three ingredients suggest is that some of the variation that we see in human culture and societies and human personalities and behaviours from country to country could be somewhat affected by this parasite that's in our brains.

Natasha Mitchell: Now that's intriguing. So what do we know about how Toxoplasma Gondii affects our behaviour, humans, and we must remind ourselves we're only just an intermediate host to this little parasite. In fact it really always wants go get back to the cat where it can breed. But what do we know about what it does to us?

Kevin Lafferty: There is a group in the Czech Republic that has done several years of studies on the personality differences of people who are infected and not infected. And the results are actually quite complicated and fascinating but I'll summarise them. The thing that is most consistent across the effects is an increase in a personality trait called neuroticism, which means that infected people tend to be more neurotic. Being more neurotic is not necessarily a bad or a good thing, you don't want to be on the extreme end of completely un-neurotic or super-neurotic. If you're un-neurotic you'd never respond to stimuli and super-neurotic is not so good either.

I'm not a psychologist but I think that the easiest way for me to describe it to folks is that people tend to be more reactive, sort of dogmatic and rigid and perhaps guilt prone and these are some of the descriptors that go along with neurotic behaviour.

Natasha Mitchell: There is a very potent gender affect here, isn't there, that the parasite seems to affect the behaviour of men and women quite distinctly. Give voice to that distinction.

Kevin Lafferty: What these guys found was that women that were infected tended to have an increase in intelligence quota and men had a decrease in intelligence quota.

Natasha Mitchell: I'm clearly infected then.

Kevin Lafferty: Woman who were infected tended, they described them as being more warm hearted and more interested in shopping. You know I didn't write these things I just found it absolutely fascinating that these were some of the descriptions of infected women. So for men the effects of toxoplasma I think you would come to the conclusion they were generally negative from our cultural perspective. But for women it was sort of a mixed bag, hard to say whether it would be negative or positive.

Natasha Mitchell: Why did this impact, potential impact on human behaviour interest you so much because it seems to be quite subtle doesn't it given that so many of us are infected by this parasite?

Kevin Lafferty: You're right it's important to state that these are subtle differences that are only distinguishable with large sample sizes and statistics and so on and so forth. You wouldn't notice the difference in yourself probably.

Natasha Mitchell: So in a sense an infectious disease, a parasite, could operate at a civilisational scale at a population level, even if the affects are quite subtle at an individual level.

Kevin Lafferty: That's what was worrying me, yeah. And it turned out that the fact toxoplasmosis is a health concern for pregnant women means that we have fabulous data on the prevalence of this parasite from upwards of 40/50 countries. We also have data on both cultural dimensions and aggregate personalities on a country to country level. People have done large-scale surveys with many, many, many people to identify differences in culture and personalities from nation to nation.

And basically the most interesting result -- you get a very strong association between the prevalence of toxoplasma and the measure of neuroticism at the country scale. The toxoplasma explains about 30% of the variation among countries in neuroticism. Now that may sound like a lot but I should point out we wouldn't expect toxoplasma to explain all the variation and the personality traits amongst countries certainly. but toxoplasma explains more variation in that particular personality measure than social science has been able to explain by any other measures. So it really does appear to be a strong association.

Natasha Mitchell: It's an association with a great story behind it, but of course you can't establish whether that relationship is causal, whether in fact toxoplasma works at the population level like this to sort of change the average or aggregate personality of a whole population.

Kevin Lafferty: Yeah, it would be nice to be able to do the experiment but it's not that practical. When we have a correlation like this we, as you said, we cannot demonstrate causation without doing the sort of experiment that would be impossible to do at a global scale. Really what we have available to us is to link these steps in the logical chain. We know we have a parasite that gets into our brain, we know that it manipulates the neural chemistry in brains. and we know that that is associated with changes in individual personalities and the assumption is that individual personalities can affect measures of group personality at the country scale. If that's the case and we know that toxoplasma is very, very common and it varies a lot from country to country you can sort of see how the logic lines up in support of this fairly bizarre conclusion.

Natasha Mitchell: What would it mean for a culture to be more neurotic than another? What does that mean in terms of the behaviours or habits or ways of seeing the world that a culture might demonstrate?

Kevin Lafferty: So what the psychologists suggest is that more neurotic cultures tend to have more rigid role orientated societies, they tend to be more risk averse and put in political structures that deal with uncertainty. They also tend to have much stronger gender roles so you know in a more neurotic society you know men do manly things and women do more feminine things. So there are implications of course of all those sorts of tendencies to result in many different types of cultural institutions.

David Hughes: Yeah, I think Kevin has made a really interesting insight with that study where he's shown correlations between for example neuroticism in human societies and the levels of these parasites.

Natasha Mitchell: I mean is it in the parasites' interests though to infect humans and change our behaviour?

David Hughes: Not at all, we're a dead end host for these parasites, what they want to be is inside rodents and then manipulating the behaviour of rodents to get then into cats. But since they're in us, since they're here reproducing they still produce chemicals and these chemicals can affect our behaviour. Actually some people are now questioning whether we can use these to our own ends. For example people are seriously considering using toxoplasma in the control of certain psychoses like schizophrenia.

Natasha Mitchell: Really?

David Hughes: Absolutely, because they do produce stuff which changes the brains of mammals.

Natasha Mitchell: So find a pharmacological equivalent?

David Hughes: Yes, absolutely.

Natasha Mitchell: Intriguing.

David Hughes: Another thing is we are in fact and the first thing that happens when a woman realises she's pregnant her doctor gives her a test to make sure she has or hasn't got toxoplasma. Interestingly there's a group in Canada looking at the evolution psychology of this and they see that women in the first trimester are much more aversive to food, as we all know, and they have increasing levels of morning sickness, which people think is in some way adaptive. But interestingly their reaction to parasites also changes, they become much more what's called disgust prone: they dislike a lot of things which could potentially infect them.

Natasha Mitchell: So when the foetus is most vulnerable?

David Hughes: Yes, you avoid foods and you avoid sources of contamination.

Kevin Lafferty: The things that we've been talking about are really subtle personality differences, but there are some interesting studies that have shown more serious associations with pathologies. So for instance schizophrenia is strongly associated with toxoplasma, there is an abstract here at the parasitology meetings that shows that Parkinson's disease is twice as high in toxoplasma positive individuals controlling for other sorts of demographic factors.

Natasha Mitchell: Now that's a very intriguing connection, there's not a lot of public discussion about that, that the possibility of infection could create a mental illness. I think we sort of resist this idea that parasites might account for major transformations of human behaviour.

Kevin Lafferty: It's largely, you know, the subject of zombie films and it's horror movie stuff. You know fortunately in this case it's really subtle things that our society has adapted to dealing with.

Natasha Mitchell: Kevin Lafferty, should we be scared of parasites, given what they have the potential to do to our minds?

Kevin Lafferty: Well I think that we need to realise what potential they have and it will help us because we're so intimately connected to them to understand them better. I'm not sure scared is the right thing, we've been dealing with parasites for the entirety of our evolution; they are a normal part of our species' history. And one of the sort of mind games I think is interesting to play with toxoplasma -- you know, half of us are infected perhaps, and if you were to ask yourself, if I am infected and I could cure myself to get rid of my toxoplasma which is my co-inhabitant, would I want to do that or am I happy with the personality I'm sharing with my parasite?

Natasha Mitchell: Ecologist Kevin Lafferty with the US Geological Survey. He lives on a nature reserve in California and on our shores recently managed to get a few ocean surfs in between sessions at the International Congress of Parasitology. Before him, Associate Professor David Hughes.