"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

September 8, 2016

Tylodelphys sp.

There are many examples in nature where parasites are able to alter their host's behaviour in some way. More recently, some scientists have been investigating just how the parasite are altering or controlling host behaviour. Most of them had looked at the chemicals secreted by the parasites to lull the host into compliance, but the study we're featuring today looked at something different - how the behaviour of the parasite itself can affect the behaviour of the host.

Left: Histology section of an infected bully's eye from Fig. 1. of the paper (r = retina, l = lens, m = metacercariae [flukes])
Right: Tylodelphys in the eye of a common bully from this video

The star of today's post is Tylodelphys - a parasitic fluke which infects a small freshwater fish in New Zealand call the common bully. In order for this parasite to complete its life cycle, Tylodelphys must enter the gut of a fish-eating bird, which would naturally involve the unfortunate fish being eaten by the said bird. While it is in the common bully, Tylodelphys dwells in its host's eyes in the vitreous liquid between the lens and the retina (see video here).

Unlike other species of flukes which turn into dormant cysts at a similar stage of development, Tylodelphys stays active and free to roam around inside the fish's eye - which provides it with plenty of opportunity to get up to all kinds of parasitic hi-jinx. When Tylodelphys larvae are crawling around inside a fish's eye and happen to get in between the retina and the lens, this can partially blind the fish and prevent it from being able to notice incoming predators such as birds.

To examine what Tylodelphys gets up to during the day, researchers at the Otago Parasitology Lab collected some common bullies and gave them eye examinations using an opthalmoscope (yes, like the one used for your eye exam). Using the opthalmoscope, they captured a series of short videos of the infected fish's eyes at different time of day, and watched what eye flukes got up to. They also performed histology to examine if the flukes are damaging the fish's eyes.

The bullies they examined varied in how heavily infested their eyes were - this range from just having a single fluke in the eye, or it can be up to seventeen flukes, with the average being about seven. Living in a crowded eye is not good for the parasites either, as the researchers found that flukes from heavily infected fish are comparatively smaller. But despite being found in a vital and sensitive part of the host body, Tylodelphys was otherwise a relatively benign tenant - they didn't mess up any eye tissue.

Compare this with other species of eye flukes which can cause cataracts in the eye of their fish host, Tylodelphys seems rather well behaved. However, that does not mean Tylodelphys isn't bad news for the bully - just that its modus operandi is more subtle. Instead of impairing the fish's sight by damaging the eye, as mentioned the above, when the flukes position themselves in front of the retina, they act like internal blinkers. Surprisingly, fish that are more heavily infected didn't have their retina more covered up by the flukes than less heavily infected fish, which means it's not simply the sheer number of flukes that blinds the fish - it's something else the flukes are doing.

Tylodelphys  has a daily routine and shifts its position in the eye throughout the day. During day time, the flukes sit between the lens and the retina, blocking the host's line of sight. But at night, they settle down to the bottom of the eye, allowing the fish to see properly again. But if Tylodelphys is trying to get its host eaten by a predator, why doesn't it just stay in front of the retina all the time? That is probably because not all predators are the same for Tylodelphys.

During the day, the main predators of bullies are fish-eating birds (which are Tylodelphys' final host), whereas at night, the main predators are longfin eels (which are not suitable as host), so it'll be good for to the fluke if their host fish can still see and avoid the incoming predators at night. So the flukes keep this fish's eyes covered during the day, but move aside to not get in the way at night, and this seems to follow a circadian rhythm.

While this helps the fluke reach its final bird host, the reason why this behaviour manifests probably has nothing to do with trying to change the host's behaviour. As mentioned above, unlike other flukes that become a dormant cyst at this stage of development, Tylodelphys keeps growing so it needs to feed - and the only thing around to eat in the eye of a fish is the fluid in the eye's vitreous body. The partial blinding of the fish host during daytime might simply be a side-effect of the parasite's feeding routine.

So while the fluke moves around in the fish's eye to get its daily dose of eye jelly, this also produce a useful side-effect by making the host more vulnerable to fish-eating birds. Such "useful side-effects" could be how many parasite host manipulation tactics have evolved. Indeed, that is often how evolution often work; co-opting preexisting features and behaviours into new roles. To understand how a parasite affect the behaviour of its host, sometimes perhaps it is best to start with studying the behaviour of the parasite itself.

Reference:
Stumbo, A.D., and R. Poulin. 2016. Possible mechanism of host manipulation resulting from a diel behaviour pattern of eye-dwelling parasites? Parasitology 143: 1261-1267

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