Rats Manipulated to be Attracted to Cats

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I devoted a whole chapter of The Extended Phenotype to parasites manipulating their hosts to assist the parasites into the next stage of their life cycle. There’s a large literature on this, which I interpret as parasite genes finding phenotypic expression in host bodies. The logic of gene/phenotype causation is the same, whether the genes are foreign or “own” genes. Indeed, part of my aim was to break down the conceptual barrier between “own” and foreign genes. There’s an abbreviated version of the argument in Chapter 13 of the Second Edition of The Selfish Gene.

Given all that, I reproach myself for missing a lovely paper in the Proceedings of the Royal Society 2000, by a group of Oxford colleagues, which is a perfect illustration of the principle.

The protozoan parasite Toxoplasma gondii, which lives inside the cells of its host, has cats as its definitive host, and rats as intermediate host. It leaves the cat in the faeces, from where it may then be ingested by a rat. It travels from rat to cat when an infected rat is eaten by a cat.

Natural selection would therefore favour Toxoplasma genes that change the behaviour of the rats they inhabit, making them more likely to be eaten by cats. This could be achieved as a “boring byproduct” of simply making the rats sick, so that they are less adept or speedy in running away from cats. However, Berdoy, Webster & Macdonald found something much more interesting. They showed experimentally that

“although rats have evolved anti-predator avoidance of areas with signs of cat presence, T. gondii’s manipulation appears to alter the rat’s perception of cat predation risk, in some cases turning their innate aversion into an imprudent attraction.”

It’s a beautiful example, which I wish had been available when I wrote The Extended Phenotype. The altered rat behaviour is an adaptation for the benefit of T.gondii genes, specifically those T.gondii genes that express themselves in the rat brains that they inhabit.

I repeat, it is especially pleasing that this effect is achieved, not in a boring way simply by making the rats sick and therefore more sluggish in escaping from cats. Indeed, they seem to have no obvious effect on the general health of rats. Their effect is a specific manipulation of rat behaviour vis-a-vis cats. It’s as though they are pulling puppet strings in the rat’s brain. A neurophysiologist would not be surprised to discover a way of doing exactly that, either with micro-electrodes in rat brain cells or with drugs. Or geneticists could do it by genetic manipulation of rat genes. It seems that natural selection, working on protozoan genes, has achieved exactly the same thing.

 

Written By: Richard Dawkins
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42 COMMENTS

  1. I can do you one better. Leucochloridium Paradoxum not only manipulates it’s host, a snail, to climb to the top of a shrub/tree where it can easily be spotted by birds. It also transforms it’s antennae into pulsating, maggot-like appendages. The snail usually survives the attack and grows a new one to infect even more birds. The infected birds rain down the new generation of parasites all over the forest through their faeces. 

  2. “I’m now puzzled. I knew about this parasite. I thought I learned about it via the work of a certain Prof. Dawkins. Oh well.”

    Perhaps you are right. I have been known to forget things I’ve written before!

    “I can do you one better. Leucochloridium Paradoxum not only manipulates it’s host, a snail, to climb to the top of a shrub/tree where it can easily be spotted by birds. It also transforms it’s antennae into pulsating, maggot-like appendages. The snail usually survives the attack and grows a new one to infect even more birds. The infected birds rain down the new generation of parasites all over the forest through their faeces.”

    Yes, Leucochloridium is definitely in The Extended Phenotype.

  3. Satan must be manipulating those genes!  Seriously, this is an argument I’ve gotten from theists when I used this example in a discussion of the genetic evidence for evolution.  Satan is everywhere in nature, apparently, getting his kicks from genetic fiddling.  Of course these people wouldn’t touch The Selfish Gene with a ten-foot pole, so recommending books to them seems futile. 
    Richard, I wish I had your intelligence, knowledge and seemingly infinite patience with these people who just can’t seem to wrap their minds around the beautiful intricacies of natural selection.  They just drive me insane.  Anyway, thank you for elucidating this great example of the expression of parasitic genes manipulating host behavior.  It’s fascinating!

  4. I love reading about this stuff,but sometimes if not most of the time i feel to dumb to comment maybe The extended phenotype 2 would be a good idea ( a couple of reads and it all sunk in)

  5. I don’t know if “pleasing” is the word. About a third of all humans carry this parasite inside of them. You better hope your immune system doesn’t fail, or it’ll mess you up. Apparently it causes or contributes to slower reaction times, suicidal tendencies, reckless behavior, pre-natal depression, schizophrenia, and bizarrely, an increased sense of guilt. Nasty little things.

  6. There´s Wolbachia, a bacteria that can infect a wide range of species, including parasites such as mosquitoes and mites. Oddly enough, while it is just mooching off most of it’s hosts, it’s interaction with the parasitic nematodes is symbiotic (it plays a key-role in fertility for example). 

    I hope Richard has time to reply to you as well, he probably knows much more about Wolbachia and other parasites of parasites.

  7. Well, I’ve heard of this parasite via a certain Prof. Dennett in Breaking the Spell, at least I think that’s where I heard about it!

    I’m fairly certain there is also a talk by Prof. Sapolsky that includes speculation(?) about this protozoa in humans. 

  8. That’s interesting because I read yesterday on the PhysOrg website that those infected with Toxoplasma gondii are seven times more likely to attempt suicide than those who remain uninfected. See here: http://medicalxpress.com/news/….

    Also Robert Sapolsky spoke some time back on the Edge.org website that his conversations with older doctors suggested that drivers responsible for accidents due to dangerous driving had, I think from memory, four or five times higher infection rates than the general public. See hear for the video: http://edge.org/conversation/t….

  9. What an absolutely fascinating story. It suggests, as I always tell anyone who will listen, that the anthropocene is not the age of men, it’s the age of bacteria (and protozoans): always has been, always will be. Us mammals are but ephemeral icing on a huge bacterial cake.

    Although not directly related to the phenotypic expression in this case, I have always been intrigued by rat behaviour. Especially since I live in the countryside and, perhaps unfortunately, have always had ample opportunity to consider their ways.

    A few years back my gardener inadvertently caught a huge Rattus in a humane rabbit cage trap. He helpfully left the trap, complete with inmate, outside the kitchen door for me to ‘deal with’.

    I never relish killing anything, so ignored the unpleasant chore for a time. Of perhaps the ten times I passed his cage that day, Mr Rat just scowled at me, exhibiting a disdainful ‘come and get me if you’re hard enough’ attitude.

    I again passed later in the afternoon, in all respects in exactly the same manner as many times before, except that I was now carrying a .22 rifle. This time, and this time only, ratty immediately panicked: squealing loudly, running in manic circles and biting the cage wires.

    I generally don’t anthropomorphise animal behaviour, but could interpret this as nothing other than the instantaneous recognition of a firearm, and a clear fear of death.

    I was so disturbed by the event that I put my gun away, loaded Mr Rat into the Land Rover, took him for a ride, and released him a mile away. I never saw the rat again, but neither did he send a thank you note.

    How on Earth can a rodent species evolve to recognise only an armed human as an immediate mortal threat? I’ve seen rabbits do the same, but the difference was never as marked. Perhaps the rat brain is wired in such a way that it is easy for new behaviours to be acquired both via external experience, or by genetic interference as in the case with Toxoplasma. Perhaps it’s a feature which has been selected for to help with hazard avoidance (eg to quickly learn to run from men who have long objects in their hands) but which has backfired by enabling parasites to take over and, for example, make them run towards the smell of cats. Evolution is nothing if not an arms race.

    Although my example has the whiff of Lamarckism. Unless it’s a rat meme – do mummy and daddy rat teach their children about nasty men with guns?

    This was the most striking example of natural selection in action that I’ve ever seen. It left a lasting impression on me.

  10. This apicomplexan has received a disproportionate amount of time (to its favor) in our classes, because of its ubiquity in the feline population, and its zoonotic potential.  For a parasite that is typically only shed 1-3 weeks during the entirety of a cat’s lifespan, it certainly causes its share of grief in the intermediate hosts!  Just one bradyzoite or cyst can result in the shedding of millions of oocysts, and it only takes one oocyst for infection.  

    I agree that the behavioral modification in rodents is fascinating, and look forward to further research in the area.  Where schizophrenia is concerned in the human population — there is work yet to be added to this growing body of research.  As Berdoy, Webster, and Macdonald noted, their research holds potential implication for humans.  Several more recent studies have made speculations linking T. gondii serointensity and seropositivity with schizophrenic and suicidal behavior.  However to my knowledge, there is no definitive research at present.  I’ve linked to an abstract (2011) and two articles (2009 & 2010) below.  The 2009 article has an interesting Discussion section exploring possible links between the effects of proinflammatory cytokines on amino acid levels such as tryptophan, and the effect on serotonin production levels in the brain.  For those interested in the possible connection between schizophrenia and T. gondii, I recommend both articles.

    - http://www.umass.edu/cns/Posto… (2009)
    - http://folia.paru.cas.cz/pdfs/… (2010)
    - http://www.ncbi.nlm.nih.gov/pu… (2011)

  11. Dennett refers to a fluke that manipulates an ant into walking up a blade of grass to be eaten by a sheep, which is the same kind of thing as what Toxoplasma is doing here, but I don’t recall that he specifically refers to Toxoplasma.

  12. One minor niggle Sjoerd.
    When writing a species name, the specific name (the second of the 2 part binomial) is always written in lower case. So…

    Leucochloridium Paradoxum, is written Leucochloridium paradoxum.

  13. Embracing anthroporphism to the full: 

    I am Super Rat.  I’m not scared of no kitty-cat.  Come and get me if you dare!  I’ll rip your whiskers off!!!  Hey guys, try this, it’s really good shit….
    … famous last words?

  14. Mark Ribbands should not worry about his story having the whiff of Lamarckism because there is increasing evidence in many forms of life that inheritance of acquired characteristics is real. In my view it provides a much more realistic explanation for evolution than purely “survival of the fittest”. I do accept the latter has a major role, such as in Mr. Dawkins example.

    Another example similar to Mark’s experience is that newly hatched geese have been shown to react with alarm to sillouettes of predator birds while being unconcerned at sillouettes of other birds.

  15. Thank you, David, for you interest.

    Superficially at least, I can think of only three explanations for my rat’s behaviour:

    1. That this individual rat had been engaged by armed humans one or more times before, but survived. This is unlikely: most people in the English countryside are quite good shots, and only very few of them enjoy the company of rats.

    2. That the avoidance of armed humans has evolved by the ‘normal’ process of random mutation and the subsequent non-random selection for a trait. Intuitively, it feels unlikely. An immediate fear of humans, sure – rats who always immediately panic when seeing these bipedal giants certainly would survive to have more rat children.

    But the likelihood of the trait of being very afraid of only those humans with long objects in their hands? The permutations are, intuitively at least, immense. Consider how many other variations there could be – people with long noses, carrying cups of tea, wearing fedoras, having a gammy leg, it’s endless. That the trait of being very afraid of only men who happen to have guns in their hands, appearing by random mutation, feels hugely unlikely.

    3. That, as David asserts, it’s the inheritance of acquired characteristics. If one considers that from many generations of rats, some individuals would certainly have survived being fired at, and maybe non-lethally injured, and therefore have learned that blokes with long things in their hands are potentially bad news.

    I shudder to think about it – from my earliest biology classes, back in the Cretaceous – Lamarck was considered daft: his ideas were against the natural order of things.

    This is absolutely not my subject. Does anyone on here have detailed knowledge of current research? (Or is anyone else going to the Ancestor’s Trail this weekend, and fancies thrashing out an answer over a bottle of wine or two?) :)

  16. http://www.ncbi.nlm.nih.gov/pm

    Mark – You might like to look at this website which gives an overview on some of the recent research which supports the concept of inheritance of acquired characteristics.

    I believe there is a current project with fruit flies specifically aimed at tracking the proof of the hypothesis.

    I don’t know what the Ancestor’s Trail is but it sounds like a lot of fun. I hope you find someone to discuss these issues with over the wine.

  17. I wouldn’t be too quick to ascribe this particular incident to evolution or genetics. I think it’s more likely that this particular rat has learned what firearms are, or at least what they represent. Imminent death or grievous bodily harm.

    I once read a story (sorry. definite case of source amnesia here) about a farmer that had a big rat problem. He made a habit of shooting rats in his yard from the kitchen window. After a few weeks and many a rat dead (but not even close to all of them) he found that most if not all rats on his farm had altered their habits to avoid the window. Except they didn’t just avoid the window entirely, they had mapped out and learned to avoid with surprising accuracy just the killzone. ie. the area delimited by the accurate range and field of view of the rifle/kitchen window combination.

    What I’m saying is, rats can be a clever bunch and this particular mr. rat may have been witness to a few shootings and may have learned from firsthand experience just what a rifle is and does. No genetics -apart from those that govern general learning- involved. 

    Of course it may not have been the rifle, perhaps you were walking straight at it this time, instead of passing it by. Perhaps you were intending to kill it, and thus smelled subtly different, tipping the rat off something was up.
    Perhaps, most boringly of all, it was just coincidence.

  18. I wonder why  do people find  trouble in accepting the metaphor of  a “gene machine”.I´ll look for the mentioned chapters.I couldn´t wait to read this carefully as I had a troubled week.
    It really was worth.

  19. That’s one of my favourite examples of active manipulation of host behaviour induced by its parasite! I’m currently ending my PhD thesis in evolutionary ecology, and I’m working on one of these manipulating parasites which deserves far more attention than it gets!

    This parasite is an acanthocephalan (named Pomphorhynchus laevis) that infects a freshwater shrimp as intermediate host (the one where the parasite larva grows) and a fish as definitive host (such as the chub, where the parasite grows as an adult and sexually reproduces). It is  known since decades that P. laevis is  able to manipulate the behaviour of its shrimp host in ways facilitating its transmission to the fish host by predation: the infected shrimp is attracted by light and by fish odours, and it does not hide in refuges unlike uninfected ones. This alteration makes the infected shrimp more susceptible to predation by fish, thus improving parasite transmission.

    We recently discovered that this alteration is only induced by “mature” parasites, that can establish in the fish host. Before reaching this mature stage, the parasite larva grows, but is not fully developed, what prevents it from establishing successfully in the fish. What’s amazing is that this immature parasite larva is able to protect its shrimp host against predation (the exact opposite of the manipulation induced by the mature parasite)! This protection makes the infected shrimp less prone to leave a refuge and increases its life span, thus parasite chances of survival until reaching the mature stage.
    This is a wonderful example of two adaptive opposite manipulations occuring in the same parasite, according to its infectivity to the final host. This is the link to our publication: https://www.researchgate.net/p

    These manipulating parasites really provide exciting knowledge about evolutionary biology and ecology!

  20. There was a special report about Toxoplasma on Australian TV a last weekend. Theme was shock horror: ‘What the authorities know about the danger lurking in our homes, but won’t tell us’.

    Unborn babies and very young children have died from this. Main source of infection is contact with cat faeces, probably by eating dirt or gardening without wearing gloves. On detecting contact with a suitable host the parasite can bore into the bloodstream in a matter of seconds. Playing in sandpits can be a problem because cats sometimes bury their faeces in them

    There were interviews with several women whose babies were still born owing to an initial infection in the mother while pregnant, probably from playing in a sandpit with an older child, or some unknown environmental trigger that causes the established Toxoplasma cysts to become active in the brain of the mother.

    The parasite also seeks to lodge in the eyes. It cannot be removed and frequently causes blindness. There was a claim that it is the main cause of blindness in in children some places.

    Approx 8 million Australians are claimed to be hosting Toxoplasma. Once the parasite enters the body it stays forever. (The only treatment is to donate your body to a cat food factory.) It is unknown what environmental triggers cause mind altering activity in humans, but fortunately they remain dormant most of the time. Most people are unaffected, other than occasionally experiencing flu like symptoms, and various minor mental disturbances when the parasite becomes active.

    In some men the effect is believed to be a driver of high risk driving behavior.

    One guy has a theory that most schizophrenia is attributable to this parasite. There’s evidence that rises and falls in the extent of schizophrenia in Britain correlates with the popularity of cat shows and cat breeding. i.e. The number of people whose houses tend to be overwhelmed by cat faeces.

    Other mental side effects of Toxoplasa infection in women include loving cats. Side effects in men include road rage. Not sure what the connection is on that. Knowing the damage our cat causes around the house I can see where the road rage aspect fits in. But why shredded curtains, sofas, various allergies, and the house smelling of cat piss appeals so much to women I have no idea. Part of a general unnatural tolerance for cats I suppose. In comparison all I have to do is spill a little coffee on the kitchen bench to unleash a compensating level of unnatural intolerance in the same woman.

  21. In other words, evolution is not egocentric. That’s dully obvious. Imagine the repercussions of rats evolving into un-catchable and thus inedible animals. As Lewis Thomas put it, the secret of life is death. What’s interesting here is the idea of one animal genetially engineering another, in the course of its evolution. The cat creating in the rat a certain disposition toward biologically productive death. What if we’re being similarly groomed?    

  22. Oh crikey!  It appears that what was once heresy is now evolving into accepted dogma. Isn’t science wonderful?

    http://www.the-scientist.com/?…

    ‘Recent experimental work in mice, worms, and pigs has found evidence that some degree of transgenerational epigenetic inheritance may take place.’

    Apparently it’s all under the control of long non-coding RNA, expressed from regions of so-called ‘junk DNA’ (which does not code for proteins.)

    So junk, as is so often the case, is useful after all: the genome, like all successful hoarders, has discovered the wisdom of not chucking too much stuff away. I hope my girlfriend reads this and learns.

    ‘One can begin to envision how environmental variation, by instigating epigenetic changes, could increase organismal [great idea, but it's a horrible word, Prof Morris] complexity, thus giving populations a greater chance at surviving new and perhaps permanent environmental threats. [What, like farmers with guns?] In other words, epigenetics, rather than random genetic point mutations, could provide the missing link between environmental pressure and the resulting genetic variability that generates robustness of a species.’

  23. You are both overestimating the magnitude of the parasites impact on human behavior and also diverge slightly from the way it in fact does impact our behavior.

    A condensed view of the research on this topic can be found here:
    http://www.theatlantic.com/mag

    Given this article, it can be concluded that Toxoplasma gondi-infected people exhibit:
    1) heightened reaction times
    2) lowered fear
    3) gender specific effects:
    a) males have a tendency towards introversion
    b) females lean to be more extrovert and trusting
    c) infected females seem to be more attracted to infected males
    d) males develop a higher tolerance to the odour of cat pee (i.e. it is less repulsive to them)
    e) females seem to be afflicted otherwise
    And perhaps more which I forgot to mention (and also one important one which you mentioned – that is, that it can be lethal to developing pregnancies and young children – so basically specimen with a weak immune system). It also seems to be very tightly linked with schizophrenia.

    From the parasites life-cycle point of view, where the shortest and I guess the most prefered path would be to only include a rat and a cat, all this influence seems to me as a very sophisticated way of delivering the parasite back from the human into the rat-cat cycle.

    Both points 1) and 2) have a direct chance of increasing the mans (and womans) probability of getting killed. I imagine that that is supposed to raise the chance of spreading the parasite to the rat by means of devouring the carcass. If given the right environmental conditions I also think points 3a) and 3b) have the same function.

    The heightened attraction between infected people could be considered natural since it has been shown with rats, that about 60% of fetuses inherit the parasite – however no data has been published yet to justify this claim in humans – it is now work in progress. This scenario is however, I think, very plausible because it’s most preferable for the parasite itself – it has a direct chance of killing the host and therefore closing the cycle as opposed to only increasing the chances of death.

    On the other hand, the killing of the host could be a bad move considering basic game theory, where, given the consequences of not doing so, it would enforce an opponent to undertake drastic measures to fight the parasite, i.e. developing a cure that kills it (which is exactly what we humans do when a woman gets pregnant – we try to kill the parasite even before the pregnancy starts – and that’s also why women are told to avoid litter boxes while being pregnant, as a possible source of infection). It may therefore be more preferable to be an almost negligible factor of impact on the general death toll but having a large basis of carriers (and lower opposition) – perhaps raising chances of success.

    The gender different behavior with regard to cat pee is a mystery to me but I don’t think it’s accidental just as well as the others are not. However, rats where almost drawn to cat pee after infection – they found it near ‘sexy’ since it aroused them sexually. Since the needs for arousal are different both in human males and females the dissonance may be a consequence of action of the same agent on a differently working system. It would be interesting to see if cat pee had the same affect on both genders of rats.

    The picture drawn above is both fascinating as well as disturbing at the same time. How much ‘me’ indeed exists within me and how much am I just a vehicle for extremely sophisticated organisms who are in fact at the wheel? And there seem to be a lot more of those then we would like. But, in the case of Toxoplasma gondi – the effect is a lot more subtle then you (as well as perhaps I) make it sound. It may not turn an introverted woman into an extrovert – it way only shift her character a bit in that direction, not change it drastically – but given the rate of infection in the population (can’t remember exactly – I think it may have been 1/4 of the entire population) it may just be the edge allowing the organism to survive.

    I wonder if rats have developed particular taste for parts of the human body? If so, it would be preferential for the parasite to settle in these regions more then in others. It would also be an indication that all the above given influence is not just accidental but has the sole purpose of making rat food out of us. If it is only incidental, which may be the case, one may wonder how universal the effect is and if it may be perhaps extended to other species? I guess it would be even more interesting to investigate this in other species if it was not incidental.

    Thank You Richard for bringing this extremely interesting topic to my attention.

    Best regards,
    Mike

  24. Was interested in your story. Now, beside simply being a case of human pattern creation in an event that is just coincidental, have you considered the fact that it was the smell of the gun. Is it more likely that a rat would witness its companions death from a weapon and learn the smell associated, while still be being hidden and safe rather than visually seeing the attacker. I had some pet rats and I can confirm two things; they have a very good sense and use of smell, they learn fast. Worth thinking about, but could make your first point just as viable.

  25. Hi dvrs.

    Yours is an absolutely brilliant hypothesis, and totally convincing. Like all the finest insights it’s screamingly obvious once stated. I’m mildly embarassed not to have thought of it myself.

    I had a colleague at the site in question at the time who, in his capacity as armourer, maintained a large stock of weapons with some kind of horrible stinky stuff which even I, with my sub-optimal human sense of smell, complained about when he was spraying it around my workshop.

    So all the guns at the place will smell the same, and smell badly.  It’s a fascinating hypothesis, and I think very possibly correct. 

    If I had the time, and some more captive rats, I could investigate with rags sprayed with gun oil and various other substances as controls. Is there anyone in Norfolk, UK, pursuing a research degree in animal behavior who needs a project? :)

  26. What is the mechanism or process which would initially enable a parasite to manipulate the perception of a rat to be attracted to its predators? Admittedly, I lack the vocabulary to properly articulate my question. What I am trying to get at is that the complexity of identifying a rat’s behavioral apparatus and then manipulating it in such a way that the rat begins behaving in a manner which endangers its own survival strikes me as something which would require intelligence and problem-solving, which of course a parasite doesn’t have. I am suffering an acute case of irreducible complexity, secondary to ignorance. I simply don’t understand how the process of natural selection could essentially program a parasite to do something so seemingly complex. Could anyone shed some light on this question, or refer me to a book from which I might learn? I realize, of course, that such a process would come about gradually through many changes. I just can’t imagine what such earlier iterations would look like. Thanks much.

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