"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

October 10, 2023

Atriophallophorus winterbourni

In Lake Alexandrina of New Zealand lives a species of tiny freshwater snail called Potamopyrgus antipodarum. These snails are capable of alternating between sexual and asexual reproduction and can be extremely abundant. So much so that they have become invasive in many other parts of the world. Outside of their original home, they are free to proliferate to their heart's content. But back in New Zealand, these snails don't always have things go their way. They are held back by a whole menagerie of flukes which parasitise them - at least 20 different species in fact.

Top: Photo of the snail Potamopyrgus antipodarum by Michal Maňas, used under Creative Commons (CC BY-SA 4.0) license. Bottom: The metacercariae cysts of Atriophallophorus winterbourni, from Figure 1 of the paper.

These flukes have a range of different life cycles, but all of them use P. antipodarum as a site of asexual reproduction - converting the snail's insides into a clone factory and rendering it sterile in the process. These flukes might be the reason why these snails continue to engage in sex every now and then, despite asexual reproduction being much more efficient. Sex is necessary to maintain genetic variations - the key ingredient in the evolutionary arms race against all those flukes.

Researchers who have been studying these snails and their flukes noticed that while all 20 species of those parasite are essentially body snatchers that take over the insides of their unwitting host, one species - Atriophallophorus winterbourni - goes beyond simply messing with their host's physiology and seems to be influencing the snail's behaviour too. Snails infected with A. winterbourni tend to be found in the shallow areas of the lake. Among snails collected from the shallow water margin of the lake, they represent 95% of the infections. Is this because those areas just happen to be hot spots for snails to get infected with A. winterbourni? Or are these flukes actually coaxing the snails into hanging out in the shallows?

To figure out if there's something special about A. winterbourni, researchers compared snails infected with A. winterbourni with those that were infected with a different species of fluke - Notocotylus - to see if such behavioural change is simply a side-effect of fluke infection, or if it is something specific to A. winterbourni. The researchers did this by setting up a series of ten 5 metres long tubular mesh cages that stretched across different depth clines in the lake, from less than 0.8 metres at the shallow end to 2.8 metres at the deep end, with different sections of the cage corresponding to different levels of water depth. Using snails collected from two high infection prevalence sites at the lake, they added about 800 snails to the deepest section of each cage, and the snails were allowed to freely roam between the different sections. After eleven days, samples of snails were randomly collected from each depth level and examined for parasites.

There are some key differences in the life cycles of A. winterbourni and Notocotylus that makes them good for comparisons. Just like other flukes, A. winterbourni undergoes asexual reproduction inside the snail host, producing a whole load of clonal larvae. But unlike many other flukes, these clonal larvae stay in the snail and transform into cysts, where they wait to be eaten by a duck hungry for snails. In contrast, snails that are infected with Notocotylus release those clonal larvae into the surrounding waters, and they do so continuously over the course of about 8 months. These larvae attach themselves to vegetation or the shells of other snails, and are transmitted to grazing ducks that accidentally ingest them. Therefore, unlike A. winterbourni, their transmission is largely decoupled from the snail's own movement and behaviour.

So after those eleven days of allowing infected snails to roam in the cages, what did the researchers find? Well, snails infected with A. winterbourni were heavily distributed towards the shallow end, with over a third of the snails in that section being infected, which is over three times higher than the expected background infection level (11%). In the deepest section of the cage, A. winterbourni-infected snails were rare, representing only 3-5% of the snails in that section, and some of them were immature infections. In contrast, those infected with Notocotylus were found to have distributed themselves fairly evenly across the entire depth cline. It is unclear what exactly A. winterbourni is doing to the snails that makes them favour shallow water, but more importantly, why would they do this? What's in it for the fluke? Well, the final hosts for A. winterbourni are dabbling ducks that only feed in the shallow parts of the lake. So in order for A. winterbourni to make a successful rendezvous with its final host and complete its life cycle, it will have to prod its snail host into the shallows.

Atriophallophorus winterbourni belong to a family of flukes called Microphallidae, and there are a few other species in this family which are also known host manipulators. For example, Gynaecotyla adunca is a species that infects marine mudsnails, and it coaxes its mudsnail host into stranding itself onto beaches, which brings them closer to the crustaceans that serve as the next host in the parasite's life cycle. There's also Microphallus papillorobustus, which infects little sand shrimps (amphipods), and it alters their behaviour in a number of different ways that makes them more visible to hungry birds. Even though not all members of Microphallidae are host manipulators, it's a trait that does seem pretty common in this fluke family. Sometimes, in order to complete a life cycle, you just have to drag that snail to where you need it to be.