Halophilanema prolata

Today's parasite and host are found among the dunes on the coast of Waldport, Oregon. In this story, the host is a little bug - and by bug, I do mean it in the literal scientific sense of the word, as in a hemipteran insect - the shore bug Saldula laticollis. The parasite is a nematode called Halophilanema prolata which, when translated, means "elongated sea salt-loving thread" - which sounds like an item you can find in a specialty gourmet shop or a post on a foodie forum. The mature female worm lives inside the bug's body cavity (top photo), surrounded by her babies (bottom photo). The larval worms reach a very advanced stage of development inside their mother's uterus before they emerge into the bug's body cavity. Each larva then escapes into the sun and surf and undergoes a final molt. It then finds an attractive mate in the sand, and gets on with the business of making the next-generation of bug-infesting worms.

Post-coital, the now fertilised female climbs onto any unfortunate shore bug that happens to be passing through the neighbourhood, and starts digging in. Most of the bugs infected by H. prolata were found among clumps of rushes along a distinct line of yellow-tint sand at the high tide mark. This sand contains a potpourri of algae, microbes, and nematodes - including H. prolata at various stages of development. This is evidently a hot spot for the parasite, because in that area, up to 85% of the bugs are infected.

Now, something must be said about the habitat of today's host and the parasite. The intertidal zone is a harsh habitat, especially for both insects and nematodes. Any organisms living in such areas must be able to endure being periodically immersed in seawater, and then left high and dry by the retreating tide. The combination of saltwater, periodic immersion and exposure poses severe osmoregulation challenges, which is why despite their great diversity, comparatively few insects have colonised the intertidal habitats. But what about H. prolata?

There are nematode worms which live permanently in marine habitats, and they have bodily fluids that are the same level of saltiness as seawater so they don't suffer from osmotic stress. But H. prolata has evolved from a lineage of terrestrial nematodes which would be subjected to severe osmotic stress (just like how you will dehydrate if you are immersed in seawater for too long - the high solute concentration of seawater draws fluid from your cells). So how do they manage?

Halophilanema prolata has evolved a raincoat of sorts - its cuticle has very low permeability (very difficult for water to move through it) so that it retains its body fluid more readily than animals with more permeable body walls. This also makes these little worms very resistant to other types of chemical stress - they can survive being immersed in 70% ethanol or 5% formalin (which are usually used for pickling biological specimens) - for up to 48 hours - because as well as making it difficult for fluid to diffuse out, a cuticle with low permeability also makes it difficult for other liquid to diffuse in.

So the next time you are at a beach, think about the little insects which are running around with nematodes swimming in their innards, and the microscopic worms getting it on underneath your feet. Why would you want it any other way?

Image from the paper by George O. Poinar Jr.

Poinar Jr, G.O. (2012) Halophilanema prolata n. gen., n. sp. (Nematoda: Allantonematidae), a parasite of the intertidal bug, Saldula laticollis (Reuter)(Hemiptera: Saldidae) on the Oregon coast. Parasite and Vector 5:24

Ligula intestinalis

The star of today's post is a fish tapeworm call Ligula intestinalis, and today's post is about a recently published paper that resulted from a 20 year-long study that monitored the presence of this parasite in the fish community of a reservoir in north-eastern France. The reservoir was originally created in 1986 for buffering the thermal discharge of a nuclear power plant, and data about parasitism of fish in the reservoir have been recorded since 1991. The main parasite infecting fish living in the reservoir is the tapeworm Ligula intestinalis. This parasite infects many different species of freshwater fish, but it mainly parasitises cyprinids (the carp family) such as carp, roach, and dace. A fish becomes infected through eating infected copepods and once inside the fish, the tapeworm develops into a larval stage call a plerocercoid in the fish's body cavity, which goes on to infect fish-eating birds such as herons and cormorants. As you can tell from the photo, the plerocercoid can reach alarming size and mass.

Over the 20 years since records were kept about parasitism of fish in that reservoir, L. intestinalis had progressively shifted its preferred host from roach (Rutilus rutilus) to silver bream (Blicca bjoerkna). The data from this study provide a picture of how this host transfer occurred over the two decades. Prior to 1998, the tapeworm was commonly found in roach and only occasionally found in other fish such as bream. But the roach population suffered from a series of sharp declines during the two decades - once in 1993, and then a more severe collapse in 1997. It was after this second decline that everything changed - in 1998, L. intestinalis began showing up frequently in bream.

It is more surprising that the switch hadn't occurred sooner - the bream made an ideal host for L. intestinalis in the reservoir. Not only was it abundant when the roach population collapsed, it was also more resilient to environmental stressors - such as thermal effluents from a nuclear power plant. Although the reservoir was restocked with additional roaches for anglers in 2002 and 2004, by that time, the parasite had already made the switch to having bream as its preferred host, and it was only found sporadically in roaches - the original host. So even though it seems as if the sliver bream made the ideal host for L. intestinalis in that reservoir, it took a dramatic event - the collapse of the roach population in 1997 - to bring them together. Ligula intestinalis adapted to changes in its circumstances by making an occasional host (bream) into their main host of choice.

Another interest finding of this study was the way L. intestinalis exploits the bream host. The tapeworm adopts a different strategy depending on the host's sex. When L. intestinalis infects a female fish, it diverts resources from her reproductive tissue, but if it infects a male fish, the tapeworm obtain nourishment from the fat reserves. This corroborates earlier studies that found L. intestinalis infection inhibits the reproductive capacity of its host.

But, the most surprising finding was that despite the grotesquely large size of the tapeworm compared to its host, the overall health of infected fish was not noticeably different from uninfected fish - which is remarkable when you consider how many resources the worm has to drain from the fish in order to grow so large. The fact that L. intestinalis was able to divert energy from the fish without compromising its health suggests that it is capable of manipulating the host's physiology with great finesse - fine tuning the physiology of its host in a way that diverts as much energy as possible for its own growth, but at the same time keeping the host alive long enough for it to be eaten by the parasite's next host.

Image from: Trubiroha et al. (2009) International Journal for Parasitology 39: 1465–1473

Reference:

Vanacker, M., Masson, G. and Beisel, J-N. (2012) Host switch and infestation by Ligula intestinalis L. in a silver bream (Blicca bjoerkna L.) population. Parasitology 139: 406–417.

Lysiphlebus fabarum

Recently there was a widely circulated study about fruit flies consuming alcohol to fight off parasitoid infections. But there are other methods that insects employ to fight off attacks by parasitoids, and the defence employed by aphids against one of its parasitoids - Lysiphlebus fabrum - is multi-layered in more ways than one.

From the parasitoid's perspective, bigger aphids provide more resources - but they are also more dangerous to tackle. Larger aphids can deliver a mean kick against parasitoid wasps, and they also have a more well-developed innate immune system, so even if the wasp can get past the kicking limbs, her eggs may not survive even if they do make their way in. Small aphids are much easier to attack and subdue and have weaker immune systems. But, because of their smaller size, they are also more likely to die from the trauma associated with being stabbed with a wasp's ovipositor, and this would end up being a waste of time and resources for L. fabarum. Therefore, much like Goldilocks, L. fabarum usually selects for the intermediate-size aphids - not so big that they put on too much of a fight, but not so small that they might not even survive the initial infection process.

However, there's another thread weaving through this story and that thread is coevolution. The effectiveness of the aphid's immune system depends on its genetic lineage. In typical co-evolutionary arms race fashion, there is considerable genetic variation in the aphid's innate immune system and certain aphid clones are better at fighting off parasitoids. But just when you are getting comfortable with the idea of aphid resistance being based on a combination of aphid age and genotype against the adversarial wasps, it's time to throw in another factor to complicate the story - the appropriately named bacterial symbiont Hamiltonella defensa.

Some (but not all) aphids carry this protective symbiont, which acts as an internal guard dog (guard germ?) that enhances the aphid's ability to kill off parasitoids. To complicate the picture further, H. defensa itself has acquired this ability by incorporating a toxin-producing gene into its genome that originated from a virus. Not only does this toxin-producing microbe kill off the parasitoid larvae inside the aphid, they also affect the egg-depositing behaviour of the parasitoid. And much like the aphid's innate immunity, age also plays a role in modulating the defense conferred by the symbiont. Younger aphids have smaller populations of H. defensa to start off, but they increase as they got older, and the more symbionts an aphid has, the better it is at fighting off parasitoids.

So how does this affect the evolutionary pathway of L. fabarum? Researchers found that because H. defensa play such a major role in the aphid's defense, not only are the wasps locked in a coevolutionary race with the aphids, they are also engaged in an even more intense arms race with the H. defensa symbionts carried by the said aphids. Even when H. defensa do not outright kill the L. fabarum larvae, they do still incur a cost; in aphids carrying the symbiont, the wasp took longer to develop, and also emerged slightly emaciated compared with those that infected H. defensa-free aphids.

The most remarkable finding that emerged was when researchers looked specifically at the different strains of symbionts and their interactions with different lines of L. fabrum. For example, they found that one particular strain of H. defensa that they called H323 conferred protection against most lines of L. fabarum - but offered the aphid no protection against one particular line of L. fabrum. Even the star performer out of all the symbionts - strain H76 - that conferred the greatest protection on average against almost all the lines of wasp tested - had a nemesis. A different genetic line of L. fabarum was able to weather the bacterial guardian's toxins and successfully develop to maturity.

What emerges is a complex series of coevolution that is occurring not just between different genetic lines of aphids and wasps, but also between the wasps and the symbionts carried by the aphids. While superficially, it may seem like the story of a coevolutionary arms race between aphids and wasps, given the strong interactions between the wasps and the bacterial symbionts, it is much more a story of coevolution between L. fabrum versus H. defensa, being played out on an "aphid stage."

Image from figure in the paper.

Reference:

Schmid, M., Sieber, R., Zimmermann, Y-S. and Vorburger, C. (2012) Development, specificity and sublethal effects of symbiont-conferred resistance to parasitoids in aphids. Functional Ecology 26: 207-215