"So, naturalists observe, a flea has smaller fleas that on him prey; and these have smaller still to bite ’em; and so proceed ad infinitum."
- Jonathan Swift

July 2, 2018

Dicroceolium dendriticum (revisited)

The lancet fluke (Dicroceolium dendriticum) is one of the most well-known and oft-cited example of parasite host manipulation. But in most people's mind, it often gets mixed up with the Cordyceps zombie ant fungus, which is understandable given that they both (1) manipulate an ant's behaviour, and (2) makes it climb onto vegetation. But that's where the similarities ends.

The lancet fluke and the zombie ant fungus are very different organisms, with very different plans for their ant host. First of all, the lancet fluke is a a type of parasitic flatworm which infects three different host animals throughout its life cycle - unlike the fungus which only infect the ant. And whereas the zombie ant fungus kills its host once it has reached the desire location to disperse its spore, the lancet fluke's endgame is to use ant as a way of reaching a mammal's belly, and it will make the ant repeat the climbing routine until that is accomplished.

Top: Internal structure of a lancet fluke-infected ant. Bottom: Internal structure of an (A) infected and (B) uninfected ant's head. Labels: emc (encysted metacercaria), nmc (nonencysted metacercaria), oe (), sog (suboesophageal ganglion)
Images from Figure 2 and 3 of the paper
In order to understand why lancet fluke does what it does to ants, let's look at its life cycle. The adult fluke lives in the bile duct of herbivorous hoofed mammals such as cattle, sheep, and deer. The adult fluke can produce hundreds or even thousands of eggs per day. These eggs are release into the outside world with the host's faeces, and some of them are swallowed by land snails.

The parasite turns the snail into a biological factory that churns a clone army of fluke larvae, which are packaged by the dozens into slime balls. These slime balls ooze out of the the snail's body, and are gobbled up by ants which find them to be an irresistible delicacy. Inside the ant, the parasite turns into what's known as a metacercaria and waits to be eaten by the final host. Given the final hosts of the lancet fluke are grazing mammals - none of which are particularly fond of eating ants - how is this parasite supposed to complete its life cycle? The lancet fluke solves this problem by making the infected ant climb onto and clamps itself to a bit of vegetation that such herbivores would eat, such as a blade of grass or a flower.

Unlike the zombie ant fungus where the ant stays locked in place and perishes once it has been moved into position, the lancet fluke will adjust the ant's behaviour depending on circumstances. If the surrounding temperature gets above 20ºC (68ºF), the parasite's spell wears off and the ant goes back to acting normal, since a hot sun-baked host is also bad for the parasites inside it. Once the temperature drops, the ant goes back to being in the parasite's thrall. While this striking example of host manipulation is well-known, exactly how the lancet fluke does that is a bit of a mystery.

The development of X-ray micro-computed-tomography, also known as microCT, has enable scientists to peer into the interior structure of many organisms, allowing them to, in a sense, perform a "virtual" dissection without inadvertently disrupting or displace the internal structures as a part of the dissection process. I've previously written a blog post about scientists who used microCT to visualise the root network of a body-snatcher barnacle, in this study another group of researchers applied the same technique to look at the lancet fluke in its ant hosts.

The researchers collected some ants from Cypress Hill Interprovincial Park in Canada, at a site which is known to be home to the lancet fluke. When the looked at the internal structure of the infected ants using microCT, they found that the parasites distribute themselves throughout the ant's body in a very specific way. When an ant eats a slime ball, it swallows a batch of genetically identical parasite clones, most of which will take up resident in the ant's gaster (its abdomen) and become "encysted" - curled up and wrapped in a protective membrane. But no matter how many lancet flukes the ant ends up with, there is always one unencysted larva which is embedded in the ant's head - specifically underneath its suboesophageal ganglion (SOG).

The SOG can be considered the cockpit of an ant - it is a control hub responsible for regulating the ant's behavioural patterns. Unlike its clonal sibs which are wrapped up in a cyst and walled off from the outside, this "head fluke" can continue to interact with and push the ant's neurological buttons from the SOG. Exactly what kind of physiological exchange is taking place between the parasite and the ant's brain has not been determined at this point, but it seems pretty clear that this "head fluke" plays an important role.

But being able to control the host come at a significant cost for the fluke. Unlike its clone mates which are enclosed in a protective coat, the "head fluke" has to sit naked and exposed because it needs to interact with the ant's brain. The cyst wall is what allows larval lancet flukes to survive passing through the final host's digestive system, and the exposed unencysted manipulator parasite will not survive this journey. So in order to bring an ant to a grazing mammal, one little lancet fluke sacrifices itself so that its clone mates will have a prosperous and productive future.

Reference:
Martín-Vega, D., Garbout, A., Ahmed, F., Wicklein, M., Goater, C. P., Colwell, D. D., & Hall, M. J. (2018). 3D virtual histology at the host/parasite interface: visualisation of the master manipulator, Dicrocoelium dendriticum, in the brain of its ant host. Scientific Reports 8(1): 8587.

6 comments:

  1. Using imaging to see inside a body is all the better but at such small scales? perhaps something new? To see the tiny things in bodies... a new application of imaging technology. Perhaps more could be done using other imaging technologies - seeing inside in real for movements. As goes imaging perhaps the use of radiation to see parasite movements. Radiation is used with antibodies to detect tumors and so with parasites to. Has this idea been pitched yet?

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    1. The preparation required for the microCT imaging would require the tissue be treated with preservative/fixative solution and phosphotungstic acid stain it, so it is not applicable for live samples.

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  2. It's Ophiocordyceps that manipulates ants, not Cordyceps

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    1. In this context, I used "Cordyceps" as the name most commonly recognised by a general lay audience as the "zombie ant fungus" (hence "Cordyceps" was not italicised there)

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  3. I am wondering why this whole lifecycle is so complicated? Why did evolution create such a complex process? Why should this happen exactly like this? Why eggs leave mammal if the final aim is to get back? I cannot see the exact role of the snail? Help me understand, pls!

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    1. That's actually one of the central questions in the study of evolutionary parasitology. Despite seeming to make things more complicated than it is necessary, complex life cycles has actually independently evolved in different lineage of parasite, showing that there must be some kind of benefit to it, despite making things more complicated.

      There are many research papers, review papers and book chapters that have been devoted to exploring this question, but the short answer would be that each host serves a different purpose. In the case of parasitic fluke, the first intermediate host (the snail) allows the fluke to undergo asexual reproduction and bolster their numbers, while the final host (a vertebrate animal) is where sexual reproduction takes place and allow the lineage to maintain genetic variability.

      Basically, different host gives the parasite access to different resources and benefits throughout its life time, with some acting as a source of nutrient for growth, another as a mean of dispersing itself across the landscape, another as a site for reproduction.

      For a more academic treatment of the topic, on the evolution of parasitism itself and complex life cycles, see also:
      Poulin, R. (2011). The many roads to parasitism: a tale of convergence. Advances in parasitology 74: 1-40.

      Accessible here: https://www.otago.ac.nz/parasitegroup/PDF%20papers/Poulin2011-AdvP.pdf

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