Himasthla elongata

Photo taken by and used
with permission from Kirill V. Galaktionov

Today's post is bit of a trip down nostalgia lane for me, as the experimental model used in the study we are featuring today is a host-parasite combination similar to one I worked on for somes years during my PhD and postdoc - bivalves and flukes (specifically flukes from a family called the Echinostomatidae - identifiable by their fetching array of collar spines). Much like a parasite that I worked on (Curtuteria australis), Himasthla elongata encysts in the foot muscle of its host and transforms into a stage called the metacercaria (see left photo). But whereas C. australis infects cockles on the mudflats of New Zealand, H. elongata infects mussels on the rock shores of the White Sea.

By embedding itself in the mussel's foot, this parasite hinders the mollusc's ability to move and produce the all-important byssus threads that anchor them to rocks or other substrates. If it becomes infected with too many H. elongata, the mussel loses its ability to use its foot and its survival becomes compromised. Thus this parasite selects for the evolution of mussels that are resistant against it, resulting in a coevolution arms race between the mussels and H. elongata.

To find out how parasites and mussels fare against each other and the role that genetic variants in both the parasite and host population play in coevolution, a group of Russian researchers conducted a series of parasite survival studies and experimental infections. First of all, they did an in vitro experiment where they exposed the infective larval stage of H. elongata (called cercariae) to the blood of different mussels. This was followed by an experimental infection study where they exposed some of those same "blood donor" mussels to H. elongata larvae and measured how well they were they at resisting the parasite.

Photo taken by and
used with permission
from Kirill V. Galaktionov

The researchers obtained parasite-free mussels from an experimental aquaculture farm to act both as blood donors and infection targets for H. elongata cercariae, while the parasites themselves came from infected periwinkles that the researchers collected from an intertidal inlet. These periwinkles harboured the asexual proliferative stages of H. elongata which produce cercariae (see photo on the right). Because H. elongata undergoes asexual multiplication in the periwinkle host, the researchers were able to obtain multiple genetically-identical (clones, essentially) cercariae from each infected snail and test them against a group of genetically-varied mussels.

The researchers paired up 51 different H. elongata clonal lines to blood samples from 161 randomly selected mussels for a total 764 parasite versus host blood combinations* (!). They found that a handful of mussels had blood that killed every single cercaria that came in contact with it and another handful had blood where all the cercariae survived and successfully turn into metacercariae. It seem that H. elongata is adapted specifically to surviving contact with mussel blood (just that it seems that some are better adapted than others), because when they tried to incubate H. elongata cercariae in the blood of the soft-shell clam (Mya arenaria), all the cercariae died within an hour or two.

In a follow-up experiment, they selected 39 of those mussels that had previously served as "blood donors"and exposed each to one of twelve H. elongata clones that were used in the in vitro experiment and found that the results of the in vitro experiment were pretty good indicators of the outcome of those experimental exposures - mussels with blood that killed all the H. elongata they came in contact with were also better than most at fighting off infection by the parasitic fluke. The rest of the mussels were fairly vulnerable to H. elongata and a small handful offered almost no resistance. The larger mussels were generally better at fighting off the parasites with just a little over a quarter of the H. elongata cercariae getting through, while more than half of the cercariae successfully established in the smaller mussels, regardless of the host or parasite genotype.

The parasites themselves also varied in their effectiveness at infecting mussels. Most of the H. elongata clones were fairly good at it, there were a few "superstars" that were especially effective at becoming metacercariae in mussels, while there were also a few "duds" that were hopeless, regardless of which particular mussel they were up against.

Other host-parasite coevolution arms races operate under so-called "gene-for-gene"-type interaction. Examples of which include the bacterial parasite Pasteuria ramosa in waterfleas where a specific parasite strain is most successful at infecting a specific host strain, or the arms race between parasitoid wasps and aphids' protective symbionts where you have wasp lines that can overcome most of aphid protective symbiont strains out there, but remain vulnerable to one specific strain of the symbiont.

What those Russian scientists found with the mussel-Himasthla elongata system does not seem as absolute. Instead, we see variation in overall performance in the population of both host and parasite: there are parasites that ranged from being super effective at what they do, all the way down to complete duds and everything in between. They in turn are going up against mussels with varied level of resistance against them, and how much of a fight those bivalves put up can also be affected by the age and/or body size of the host. However, what it does have in common with those "gene-for-gene"-type coevolutionary systems is that there is a genetic component to either infectivity or resistance, and none of the host are completely resistant to all parasites, just as not all the parasites are completely effective at infecting the available hosts.

Reference:
Levakin, I. A., Losev, E. A., Nikolaev, K. E., & Galaktionov, K. V. (2013). In vitro encystment of Himasthla elongata cercariae (Digenea, Echinostomatidae) in the haemolymph of blue mussels Mytilus edulis as a tool for assessing cercarial infectivity and molluscan susceptibility. Journal of Helminthology, 87: 180-188.

*because there was simply not enough blood and cercariae to go around, not every H. elongata clone was exposed to the blood from every mussel

Urogasilus brasiliensis

While most people who have some passing familiarity with copepods would know them as tiny zooplankton crustaceans, a large number of them are actually parasitic. In fact, about a third of all known species of copepods are parasites and with about 13000 known species of copepods in total, that is a lot of parasitic species. These parasitic copepods infect a wide variety of aquatic animals and come in all kinds of weird shapes.

Photo composed from Fig 4 and Fig 5 of the paper

Naturally, many of them are fish parasites as fish are such an abundant and diverse group of aquatic animals. But while most parasitic copepods of fish usually infect the skin or gills of their host, today's parasite stands out from the crowd as it inhabits the fish's urinary bladder and is the first parasitic copepod ever known to live in that organ.

Now that is not to say that a fish's bladder is a parasite-free zone - far from it. You wouldn't think that an organ that gets periodically filled up with urine and metabolic waste would be prime real estate, but there are all kinds of parasites that call it home ranging from single-cell eukaryotic parasites, to myxozoans, parasitic flatworms like monogeneans and digenean flukes - some of them are even found exclusively in the urinary bladder. However it is an unusual habitat for a parasitic copepod seeing how, as mentioned above, most live on the fish's skin or gills

Today's featured parasite, Urogasilus brasiliensis, is a newly described species that has been found in some freshwater fish living in the Cristalino River, a tributary of the Araguaia River in Brazil. The known hosts to this parasite include the tiger fish and two species of peacock bass. Much like other parasites that infect many different species of hosts, some hosts are just better than others and that is the case for U. brasiliensis too. This copepod tends be more common in the tiger fish and grows to a larger size in that host, indicating that it is possibly a better host for the parasite than the peacock bass. But while U. brasilensis is not particularly picky about what species of fish it infects, it is picky about where it lives within that fish - it is always found in the bladder.

Living in the urinary bladder does present some physiological challenges - as mentioned above, it is an organ that regularly alternates between being empty and being full of urine. Such periodic shifts in the concentration of fluid surrounding U. brasiliensis would cause severe osmotic stress like those experienced by animals that regularly migrate between freshwater and marine habitats. Presumably U. brasiliensis has overcome this particular obstacle and in doing so has been able to colonise an otherwise fairly vacant niche not occupied by other parasitic copepods.

Urogasilus brasiliensis is one of the few parasitic copepod that has evolved into an endoparasite (internal parasite) as opposed to being an ectoparasite (external parasite). But it is not alone - a few other species of copepods have also evolved to conquer that frontier, some of which we have featured on this blog such as one that lives in the cephalic canal of fish in Australia and another species lives in the rectum of rockfish.

Reference:
Rosim DF, Boxshall GA, Ceccarelli PS. (2013) A novel microhabitat for parasitic copepods: A new genus of Ergasilidae (Copepoda: Cyclopoida) from the urinary bladder of a freshwater fish. Parasitology International 62: 347-354