Wednesday, July 11, 2012

'The Good, the Bad and the Ugly: Evolution and Life History of Parasitism' at the Zoological Society of London , 11th July 2012


It’s a lovely sunny day and you’ve decided to go and see the sea.  You stand on a clifftop, feeling the salty breeze gently wafting around you.  You stare at the sun sparkling on the surface of the water.  It’s such a beautiful day.  The water.  The water looks so inviting.  The water looks so close, almost like you could reach out and…  Before you know what you’re doing you’ve leapt into the void.  A moment of weightlessness, and you slap into the water like a paper bag full of meat.  Pain courses through your body, you try to swim for the surface but your shattered limbs just won’t respond, it’s like you’re trapped in syrup.  You open your mouth to scream but you just gurgle weakly as something - SOME THING moves inside you.  Unblinkingly you stare down at yourself and watch in mute horror as it begins to uncoil itself from your body.  Long, slimy, writhing around, it just keeps coming out of you.  Like an sickly animated piece of string it keeps unravelling itself from your gut.  It wriggles obscenely and is finally free.  You feel light-headed and faintly watch it swim off into the murky water.  The last thought that runs through your head is “why? Why?!  WHY!?!?”.

“Why?”  Because you are/were a cricket or grasshopper that unfortunately ingested the eggs of the nematomorph hairworm Spinochordodes tellinii.  Unbeknownst to you, your insect brain has been subtly reprogrammed by a worm that lurks within your guts, driving you to think that committing suicide by leaping into water is the best thing in the world.  And it is.  For the worm.  It’s now free to reproduce and live a full life.  Which is more than we can say for you, grasshopper.

Welcome to the wonderful world of parasites.

The nematode emerging
This night comprised three lectures at the Zoological Society of London (ZSL) taking place in their meeting rooms just outside the main zoo in Regent’s Park.   The world of parasites is hugely diverse - 50% of animals can be considered parasites to some degree, and a far wider range of plants and fungi rely on non-mutual beneficial relationships with other organisms.  The talks tonight focused on three specific topics.  The spread of fungal parasites across the world with an emphasis on depleted amphibian populations, the history and origins of pandemic HIV, and how parasites can manipulate the behaviour of their hosts.

First up was Dr Matthew Fisher (Imperial College Faculty of Medicine, Department of Infectious Disease Epidemiology).  The ‘fungus kingdom’ contains a bewilderingly huge number of different species, current estimates are that maybe 5% of them have been formally classified.  Fungi can function as parasites in a number of interesting and occasionally bizarre ways.  We were shown some notable examples like Ophiocordyceps unilateralis, which turns ants into so-called ‘zombie ants’, making them climb to the top of leaves, dying and releasing a cloud of spores.  We were also given a brief history of mycotoxins, specifically ergot, which killed 40,000 people in the Dark Ages and may be be responsible for the hysteria surrounding the Salem Witch Trials.  It can also be used to synthesise LSD.

A 'zombie ant'.
We were shown a model of how the relationship between parasite and host organism functions – the ‘Red Queen’ effect.  In simple terms, this explains how host organisms that are initially susceptible to a certain type of parasitism develop a resistance or defence against the parasite over time.  Conversely, the parasite will develop a way around the resistance, and the host-organism will adapt accordingly.  Essentially, to stay in the same place, both organisms must stay in a perpetual arms race to try and keep one step ahead of the other. 

Frogs dead as a result B. dendrobatis infection
But this equilibrium is in danger of being upset.   With the advent of commercial air travel, organisms can now spread around the planet vastly quicker than they ever could in the past.  In particular, amphibian populations worldwide have plummeted due to the fungus Batrachochytrium dendrobatis.  This fungal infection rapidly spreads when the spores come into contact with the surface of the amphibian’s (generally frog’s) skin, causing sloughing, redness, ulceration, roughening and eventually death.  Historically, such a lethal parasite should not be able to spread very far – an organism that kills off it’s host so quickly tends to be limited by distance, but with frogs being transported around the world for pets, zoos and food it has spread worldwide, with catastrophic population declines (even in some instances, extinctions) in North, Central and South America, Australia, and the Caribbean.   

White Nose syndrome
It make for fairly scary set of statistics, and it’s astonishing how quickly the right sort of fungal parasite can rip through a population of animals.  It’s not just frogs either.  Fungal parasites have been fingered as the culprits in Colony Collapse disorder in Honey Bees, and in White Nose syndrome in bats – both of which have suffered huge population declines.  It underlines the importance of biosecurity, something which, in today’s world may, unfortunately, be approaching the impossible.  Someone walks through a field in Thailand and spores get stuck to their boots, and then they get on a plane and a day later are walking through the streets of San Francisco or London.  The notion of a global community has made the world a much smaller place, and these are just some of the consequences we have to face.

Colony collapse disorder
Next was a talk by Prof Dorothy Crawford (Centre for Infectious Diseases, University of Edinburghabout the history of the spread of pandemic HIV.  It is initially a shock to think of ourselves in the middle of an ongoing pandemic.  The notion of a pandemic is breathlessly explained by sensationalist media as a sudden and world-changing event.  However, much like the frog that is boiled alive as the water slowly heats, we are in the middle of a worldwide, slow burning disaster.  I suppose familiarity breeds contempt.  HIV/AIDS related news rarely makes the news these days, despite there being a 3 million a year death toll.  It seems to be regarded as something that happens to 'other people', and even though we are aware of the epidemic in Africa it seems distant to us.  

Artist's representation of HIV
What this lecture did was show us how scientists have traced the vectors of the disease back to its place of origin.  This is a scientific detective story, and shows some fantastic deduction and application of practical knowledge.   When AIDS/HIV was first identified, similarities were quickly noted to the Simian Immunodeficiency Virus (SIV), and a link to Africa was quickly established.  There are 12 variants of the HIV virus, and the variant HIV-M is the only one that has gone global.  Genetic sequencing traces this  variant back to the equatorial region around the countries of the Democratic Republic of Conga/Gabon/Republic of Congo and specifically to the area around Kinshasa.  But how did the virus leap from simians to humans?

Looks delicious.
Likely answers seem to point to the use of chimpanzees as bush meat.  It is plausible that while butchering an infected chimpanzee, a person with an open wound inadvertently got infected blood on it.  Other possibilities could be that it was transmitted via a pet bite, or possibly through inter-species sexual intercourse.  Science was, amazingly, able to narrow down the history of the virus even further.

Having established that the virus originated in chimpanzees, scientists set out to find which chimpanzees these were.  Obviously it is quite difficult to take blood samples from wild chimpanzees, an animal that will rip your arm off given half a chance.  So a method was devised to test for particular strains of SIV in the faeces of the chimpanzee.  By carrying out this study, they were able to narrow the source right down a particular troop of chimpanzees that live near the source of the Sangha river.  Without the presence of humans, it is likely where the virus would have remained there, but Western colonialism introduced industry to the area, and people flocked down the rivers into crowded cities.  These cities were essentially labour camps at the time, and had a highly disproportionate men to women ratio.  This naturally led to a high level of prostitution, which led to STDs, a symptom of which is ulceration - perfect transmission conditions for HIV.

Children queuing for smallpox vaccination
Another possibility is mass vaccination projects in the 50s and 60s - during these a doctor would vaccinate hundreds of people at once using an overly quick sterilisation procedure that would have proved inadequate in killing off the HIV virus.  Using all this information we can narrow down some crucial dates with some accuracy.  Scientists managed to get access to blood samples from Kinshasa dating from 1959, and 1 of these 1000 samples tested positive for HIV.    Based on this, we can can extrapolate that HIV jumped from chimpanzee to human around the period 1908-1933, with the most likely year being 1921.  It's a fantastic and impressive bit of epidemiology, and if we understand the conditions which gave rise to AIDS/HIV then it raises the chances that we can produce a viable treatment or cure for the virus.

The final speaker was Frederic Thomas (IRD/CNRS, Montpellier, France) who talked about host manipulation of parasites.  This was the most accessible lecture for a layman like myself, and also the most impressively gross.  The notion that a parasite can control another organism like a puppet on a string is highly disturbing and raises a number of questions about what is 'normal' animal behaviour. 

We were presented with numerous examples of host manipulation.  Some of the most dramatic are those in which the host organism is driven to sacrifice its life in order to propagate the parasite.  The opening paragraph of this article is a description of what Spinochordodes tellinii does to a cricket or grasshopper, but we can see parasites making creatures as disparate as cockles, mice, ants and prawns engage in behaviour that directly puts them in the path of death.  We were shown videos of animals seemingly committing suicide and the parasite emerging from them.  It's a fantastic, yet disgusting, example of the complicated path that an organism can take to get into its preferred environment.  

This cheery little fellow is D. dendriticum.
For example, Dicrocoelium dendriticum 'wants' to be inside a cow or a sheep.  So how does it get there?  Well, the eggs are excreted by a cow or a sheep, and then ingested by a snail - the first intermediate host.  The snail then leaves the parasite in its slime traces as it moves about, which are then ingested by an ant - the second intermediate host.  The parasite then manipulates the behaviour of the ant 'driving' it to the top of blades of grass, where it is likely to be eaten by a cow or sheep.  Success!  The parasite is right where it wants to be - the final host.  Journeys like this underline the importance of inter-relations in ecosystem, as well as giving us an example of the  flexibility of evolution.  As Jeff Goldblum said in 'Jurassic Park' "Life finds a way."

The current 'superstar' of manipulatory parasites is Toxoplasma gondii.  This parasite acts on rodents, making them attracted to the smell of cat urine.  Obviously this is not a great taste for a rodent to develop, and invariably ends up with it being eaten by a cat.  It's just about comprehensible for us to see a 'simple' animal like an ant or grasshopper being manipulated, but a mouse?  It raises disturbing questions about whether our own susceptibility to being manipulated by parasites.  In evolutionary terms we are far closer to a mouse than an ant, and indeed, T. gondii can be transmitted to humans.  It has been theorised that a T. gondii may be responsible for a number of human behavioural traits.  It has been linked to schizophrenia and depression.  Bizarrely, and more specifically, a man that tests positive for T. gondii apparently runs a high risk of getting into car accidents, and becoming jealous or becoming dogmatic in his views.  A woman that tests positive runs a much higher risk of committing suicide violently, becoming more promiscuous and possibly most bizarrely, of  possibly becoming more intelligent.*

A rodent with a very poor sense of survival.
We like to think of ourselves as rational actors, and the notion that some micro-organism is secretly pulling the strings is disquieting.  Can a person be held accountable for their actions if it could be proved that they would not have behaved in that way if not for a parasite behind the scenes?  Clearly the relationship between humans and parasites is one that warrants a lot of study to find out the exact ways in which they manipulate us.  At the very least, if we can understand the mechanisms behind parasitical manipulation of personalities and behaviour we should be able to formulate new and effective drugs for the treatment of mental health issues.  Maybe one day in the future a remedy for depression might be to swallow a pill full of genetically engineered worm eggs that'll infest your brain and forcibly cheer you up.  If that doesn't brighten your day regarding prospects for the future then I don't know what will.

Three interesting speakers.  Three interesting topics.  Free booze.  I think I'll be going to back to see more of what ZSL has to offer in the future.

If I've screwed any of this science up!  Scientists, let me know!

*needless to say this is all highly debatable. Interesting though.

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