Tetracapsuloides bryosalmonae

For many parasites, host castration is a very effective strategy. By specifically diverting energy from the host's reproductive functions, the parasite can horde as many resources as it can without compromising any organs or functions that are vital to everyday survival of the host. It is a strategy commonly used by digenean trematodes (parasitic flukes) and some parasitic crustaceans.

But, those parasites infect hosts that exist as discrete individuals (unitary organisms) - what about modular animals like corals and salps that live as colonies composed of many genetically identical individuals? Such organisms undergo alternating bouts of asexual and sexual reproduction throughout their life-cycle - so are there parasites that can castrate such hosts?

Today's parasite is Tetracapsuloides bryosalmonae - it is a myxozoan, parasites that were once thought to be protists, but are actually related to jellyfish and corals in the phylum Cnidaria. Throughout their evolution, they have simply been heavily modified for a parasitic way of life. Tetracapsuloides bryosalmonae has a very comprehensive scientific name in terms of describing its life-cycle - the species name encompass both of the parasite's hosts; bryozoans and salmon. In salmon, it causes a serious disease call Proliferative Kidney Disease (PKD), but less is known about its ecology in its bryozoan host

Bryozoans are also called "moss animals", and they are quite odd (even if rather common) little critters (you can read more about them on the Bogleech website here). They are colonial animals that live as a collective of individuals called "zooids", and are encased in a mineralized exoskeleton that can take on various shapes including fans, bushes, and flat sheets. Most of the time, the colony grows by budding genetically-identical zooids (clones), and colonise new habitats when fragments of the colony break off and settle elsewhere. But during lean times, the colony starts producing statoblasts, which are tough little capsules of cells that can be released into the environment to start the colony anew elsewhere, rather like seeds.

Most of the time, T. bryosalmonae exists as a quiet, secretive infection in the form of single-cells embedded in the body wall and proliferates as the colony grows. But this parasite can also switch into a more overt mode where it starts producing multicellular sacs of parasite cells, and because individual zooids are connected to each other in the colony via a common body cavity, during such flare-ups, the infection can spread throughout the colony. During the overt phase of the infection, T. bryosalmonae effectively castrates the bryozoan, and infected colonies cannot produce statoblasts.

However, on the flip side, because infected colonies aren't diverting resources towards producing statoblasts, they are better able to survive periods of starvation and suffer fewer overall zooid deaths comparing with uninfected colonies. In the natural setting, T. bryosalmonae usually enters its overt phase during late spring or autumn when the bryozoan colony undergoes its greatest period growth of asexual growth - which gives the parasite more opportunities to spread. As the parasite subsides back into its covert phase again, the bryozoan colony once again has an opportunity to produce statoblasts.

By cycling between a covert and overt phase, the parasite can persist without causing damage that can compromise the host's survival. Asexual colonial organisms can avoid permanent castration like that seen in snails infected with parasitic flukes. Theoretically, colonial modular animals can potentially live indefinitely due to their mode of reproduction. But another benefit associated with such a life-style could be an increased tolerance for infection - whereas discrete, unitary animal might be completely sterilised by host-castrating parasite, when infected with a parasite like T. bryosalmonae, modular animals can simply bide their time and reproduce when the parasite subsides between periods of overt infection.

Image from the Natural History Museum

Reference:

Hartikainen, H. and Okamura, B. (2012) Castrating parasites and colonial hosts. Parasitology 139:547-556

Diplostomum pseudospathaceum

Most animals are infected by multiple species of parasites or multiple strains of the same parasite species that are not close kin. Rarely does an individual parasite (and its close kin) gets to monopolise the resources of an entire host. So do parasites like to share? The answer to that depends on the host (and parasite) in question. Because different species often exploit a single host in different ways, a parasite can share a host with many other species without ever coming into conflict with them. But, when a parasite finds itself sharing a host with members of its own species, competition is more likely to occur as they are all going to be after the same (limited) resource (whatever that may be) from the host.

For some parasites, competition arising from coinfection can favour the most virulent strains, leading to greater overall harm to the host. But more recent studies have shown that the most competitive strains are not always the most virulent. In some cases, competition between co-occurring parasites can actually be beneficial for the host as the parasites end up mutually suppressing each other. How this plays out depends on how the parasite uses its host, and in parasites that have complex life-cycles, this can change from host to host.

The parasite we are looking at today is Diplostomum pseudospathaceum - more commonly known as the eyefluke. As with most parasitic flukes, D. pseudospathaceum uses a snail for the clonal stage of its life-cycle to make thousands of larval stages (called cercariae), which are then released into the water to infect any nearby fish. In the fish, the parasite migrates to its eye and uses it as a temporary vehicle to reach its next host - a fish-eating bird. Diplostomum pseudospathaceum essentially turns its snail host into a parasite factory, using the snail's bodily reserves as raw material to produce its army of clones. There is only so much to go around inside a snail, and when a particular D. pseudospathaceum strain has to share a snail with other strains, it ends up producing many fewer cercariae than if it had the whole snail to itself. But while it is detrimental for D. pseudospathaceum to have close company in the snail, it is a different story in the fish.

While D. pseudospathaceum undergoes a resource-hungry spree of rampant asexual multiplication inside the snail, it is relatively dormant inside its fish host. All it needs from the fish is a space to tuck into within its eye - and there is plenty of room in the fish's eye for these flukes. In fact the more the merrier given that at high numbers the eyeflukes can induce the formation of cataracts - and a half-blind fish is more likely to be eaten by a bird. But there is also another reason for D. pseudospathaceum to be more welcoming to strangers in the fish host.

The immune system of the fish is remarkably adept at responding to intruding parasites, and the immune system can be quickly "primed" towards recognising and destroying particular parasite strains. To reach the fish's eye, D. pseudospathaceum has to complete a treacherous journey through the fish's body, all while under close scrutiny and assault by the fish's immune system. In fish that have previously been exposed (and thus "primed") to D. pseudospathaceum cercariae, the chances of the parasite successfully reaching its destination are greatly diminished. But while a fish might be "primed" towards cercariae of a particular strain, a double- or even triple-prong attack is likely to overwhelm its finely-tuned targeting system. When exposed to simultaneous attacks from multiple, genetically-diverse strains of D. pseudospathaceum cercariae, the fish's immune system becomes overwhelmed, which in turn allows more eyeflukes to slip by.

In the life-cycle of D. pseudospathaceum, there is a time and place for everything - while there is a time to be on the look out for number one, there is also a time to love thy neighbour.

image by Tina Loy, modified from here

Karvonen A, Rellstab C, Louhi KR, Jokela J. (2012) Synchronous attack is advantageous: mixed genotype infections lead to higher infection success in trematode parasites. Proceeding of the Royal Society B 279: 171–176

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

Acanthocephalus dirus

The word parasite has a lot of connotations associated with it, and "maternal" is certainly not one of them. To most people, the term "freeloader" comes to mind (hopefully, this blog will show you that parasitism is actually a very challenging way of life). They also have a reputation as being pretty lousy parents. In most textbooks, parasites are usually considered as "r-strategists" - which produce many, many offspring and don't take good care of them (as opposed to a K-strategist which produces fewer offspring, but invest a lot into parental care - like an elephant). But not all parasites are bad parents, and today, I am going to tell you about a study on a maternal parasite which sacrifices everything (literally) for her offspring.

Acanthocephalus dirus has a reproductive strategy that is unusual for its group - the acanthocephalans or the thorny-headed worms (Acantho = "thorns", Cephala = "head"). In fact it is unusual compared to most intestinal parasites. Unlike some tapeworms, which profligately cast off segments (each containing hundreds of eggs) into the wilderness with abandonment, A. dirus has rather different approach. The impetus that spurred on this piece of research were two separate observations: (1) fish that are infected with A. dirus do not have any worm eggs in their feces (unlike most animals infected with intestinal parasites) and (2) perfectly healthy and intact female worms were often expelled from the definitive host. What the researchers found was that instead of simply laying eggs that are expelled from the worm and from the host, a female A. dirus actually retains her eggs until she become completely bloated with them - at which point she exits gracefully from the host fish's digestive tract. Some readers might recall a nematode that has a similar reproductive strategy, and that both lineages have evolved such a reproductive strategy independently. So why has A. dirus evolved such an extreme strategy instead of just laying eggs normally like other thorny-head worms?

One reason could be that A. dirus infects creek chub - which, as its name indicates - lives in flowing creeks. The chub acquire the worm through eating infected isopods in the stream (the picture shows the light-coloured infected isopod on the right, and the darker uninfected individual on the left), which become infected when they ingest worm eggs resting on the creek bed. Acanthocephalan eggs tend to float - so if the eggs are simply expelled into the environment, they would get washed away downstream and deposited where the isopods do not occur. Whereas with A. dirus, the worm's own body can act like a weight belt which would carry the eggs down to the sediment layer, so by the time the worm herself decays, the eggs are already in the sediment where isopods can pick them up.

Furthermore, laboratory tests showed that isopods like to eat egg-filled female worms as much as their usual food - leaf litter - and the worm body itself actually enhances the infection success of the eggs. Researchers found that when exposed to fresh eggs alone, fewer than one in four isopods became infected, whereas when exposed to gravid females, over 80% became infected (natural infection comes somewhere in between those at about 60%). By making the ultimate maternal sacrifice, A. dirus gives her offspring the best possible start in life.

Image from figure in: Seidenberg (1973) Journal of Parasitology 59: 957-962

Reference:

Kopp, D.A., Elke, D.A., Caddigan, S.C., Raj, A., Rodriguez, L., Young, M.L. and Sparkes, T.C. (2011) Dispersal in the acanthocephalan Acanthocephalus dirus. Journal of Parasitology 97: 101-105

Ascarophis sp.

When I saw the reports of giant amphipods being dragged up from the Kermadec Trench off the coast of New Zealand, my immediate thought was "I wonder what parasites it has?" This promoted me to do a write-up of a paper I've read recently, which is about a parasite that infects amphipods - admittedly those that are more modestly sized. Today, we are featuring a study on Ascarophis, a nematode worm that infects an intertidal amphipod (Gammarus deubeni) in Passamaquoddy Bay, New Brunswick, Canada. Compared with related species this worm has evolved to live the simple life(-cycle), and avoids the complications that come with having a complex life-cycle.

Previously on this blog, we have featured parasites that have evolved to take short-cuts with their complicated life-cycles. When a particular host is absent, such parasites may opt to ditch that host from their life-cycle, and switch up their developmental schedule. This is the case with the fluke Coitocaecum parvum. However, while C. parvum can switch between different life-cycles depending on circumstances, Ascarophis has completely abandoned that altogether, and has evolved to make things simpler by completing its entire life-cycle within its amphipod host. Usually, parasites with complex life-cycles use different hosts for different functions - i.e., one host might merely serve as a transport and/or resources for temporary development, whereas another acts as a mating ground and/or habitat in which it reaches maturity. So how can Ascarophis get so much functionality out of a tiny little crustacean?

Nematodes normally go through 4 larval stages (L1-L4) before becoming a sexual mature "fifth stage" worm (L5). The end of each larval stage is accompanied by a molt (rather like insects). In related nematodes that have retained their complex life-cycle, the L3 worms (which are ready to infect the next host) live encapsulated in the first host, while the L4-L5 live in the digestive tract of the final host. What the researchers found with the Ascarophis they collected from New Brunswick is that L1 and L2 worms were found in the muscle tissue, and upon reaching L3 the worms begin to migrate into the body cavity where they complete their development into adulthood and start producing eggs. Now compare this with Ascarophis from the White and Baltic Seas, which also infect amphipods, but uses a species of sculpin as their final host. Those fish acquire their infection by eating amphipods infected with L3 stage nematode, and the worms develop into adults in the fish's gut.

In effect, the Ascarophis from New Brunswick gets the most out of its little crustacean host by using different parts of the amphipod's body as surrogates for different hosts - instead of being transmitted to a different host, it simply moves to occupy a different part whose function is close enough to its needs for it to complete its development. Unlike the C. parvum, it appears that Ascarophis has abandoned the fish host altogether, and has committed itself to using the amphipod as the sole host for its entire life-cycle. Even though the Ascarophis found in the White and Baltic Seas have retained their complex life-cycle, researchers of this study suggested that they are the same species as the worms they looked at, but the New Brunswick variant has simply adapted to local condition and evolved a different life-cycle. However, it must be noted that the researchers have come to this conclusion based on the worm's morphology and as we have seen before, appearance can be deceptive with nematodes.

Through all that, this plucky little New Brunswick parasite faces one last problem - getting its eggs out of its crustacean host. For worms that live in inside a fish's gut, passing eggs out into the environment is a pretty straightforward affair - the eggs simply get washed out with the poop. But there is no exit in the body cavity of an amphipod, so how is a worm supposed to cast its eggs out into the environment? Well, this thrifty nematode simply waits for the host to die, and as the body disintegrates, the eggs are released as well. Of course, it helps that these amphipods have a tendency to cannibalise the rotting bodies of their fallen comrades - this presents the perfect opportunity for the parasite to infect a new batch of hosts - yet another reason to not gnaw on any random corpses you may come across.

Image modified from figure in the paper

Reference:

Appy, R.G. and Butterworth, E.W. (2011) Development of Ascarophis sp. (Nematoda: Cystidicolidae) to maturity in Gammarus deubeni (Amphipoda). Journal of Parasitology 97: 1035-1048.

Pasteuria ramosa

Parasitic infections can severely debilitate the host in many ways, sometimes this manifests itself as the loss of some, or even all, of the host's reproductive ability. Evolutionary speaking, an organism that cannot reproduce is as good as dead. However, it's not entirely clear who (if anyone) is benefiting from this outcome - is it; (1) a survival strategy by the host to temporarily free up resources to compensate for the parasite's presence? Or is it (2) an adaptive strategy by the parasites to divert as many resources as possible to themselves without compromising the host's ability for self-maintenance and survival? Or is it (3) merely an unintended side-effect of infection? Of course, (1) and (2) are not mutually exclusive, and in the case of (3), even if it had started out as an unintended side-effect of infection, if host castration resulted in higher reproductive fitness for the parasite, then that trait will be positively selected for and become part of the its repertoire of host-exploitation strategies.

Waterfleas (Daphnia) are infected by all manner of parasites (we featured one of them during the early days of the blog: Caullerya mesnili) ; most of them are pretty nasty - they often end up castrating and/or killing the host. Pasteuria ramosa is no different - it is a spore-forming bacterium that infects waterfleas, makes them bloated, darkening their body (see the right waterflea in the photo) and castrates them in the process. While it was previously thought that any waterfleas infected by P. ramosa were permanently castrated, it turns out that some lucky Daphnia can actually recover from their infection.

So do these little crustaceans adjust their reproductive output in response to the parasites and is castration a way for them to compensate for a (potentially) temporary hiccup in their baby-making ability? To find out, a team of scientists from Norway set out to see just who benefits the most from host castration. Their logic is that if it is an adaptive strategy by the parasite, then we should see higher spore output from a permanently castrated host. Whereas, if castration is an adaptive coping mechanism by the waterflea, then there should be a jump in reproduction upon the onset of infection as the waterflea tries to make as many baby Daphnia as possible before P. ramosa put a stop to it, then store up reserves during the infection to "wait it out".

To correct for any potential sex differences (there are many documented case of sex-bias in parasitism), these scientists used only female waterfleas for the experiment. During the course of the study, about half the waterfleas they infected with P. ramosa managed to regain their reproductive capacity. In those lucky ones, the parasite produced many fewer spores than in waterfleas that had been permanently castrated. So evidently, P. ramosa benefits from having permanently castrated hosts. But what about the waterfleas themselves? Were they able to compensate by adjusting their reproductive output in the parasite's presence?

The scientists found that by far, the strongest predictor for the lifetime reproductive output of a parasitised waterflea is the age at which it becomes infected - the later that it became infected, the more time it had to churn out babies before it came down with a severe case of P. ramosa. So it's pretty much a case of "use it or lose it". They did not find evidence to suggest the waterfleas made any effort to increase their reproductive output before they are castrated by their parasites. This is unlike other systems where parasite-castration occurs. In trematode-snail systems, the infected snails are less likely to recover from their infection. The strategy which has evolved among snails in areas with high parasite prevalence is to reach sexual maturity as quickly as possible (For example: see this study) so they can eke as many baby snails as they can before they inevitably become infected and be taken over by squirming body snatchers.

It should be noted that the waterfleas used in the experiment were from Southern Finland, whereas the parasites were isolated from a pond in Northern Germany. So perhaps the reproductive strategy of the Daphnia population used in that experiment has evolved in response to their local parasite(s) population instead. Other studies have found waterfleas to be locked in a close evolutionary race with their parasites across space and time, so the outcome of any host-parasite interaction will be dependent on the genetic identity of both host and parasite.

Image credit: Jensen et al./PLoS Biology

Reference:
Magerøy, J.H., Grepperud, E.J. and Jensen, K.H. (2011) Who benefits from reduced reproduction in parasitized hosts? An experimental test using the Pasteuria ramosa-Daphnia magna system. Parasitology 138: 1910-1915

Spauligodon atlanticus

Today, we look at a paper showing how data from DNA sequences can help resolve the evolutionary relationship of different parasite species, and even find new species where we least expected it. Traditionally, parasites - like other organisms - are classified based on key characteristics of their anatomy. However, many parasites have simplified morphology (an extreme example is the parasitic snail which has evolved into nothing but a bag of genitalia) and often the few key characters that can be examined are heavily reduced. Therefore, any conclusions about relationships between different parasite species that are based upon anatomical characteristics can lead to misleading or, at best, incomplete conclusions.

Spauligodon atlanticus is a species of nematode that parasitises Gallotia, a genus of lizards living on the Canary Islands (see image). Spauligodon atlanticus was initially described in 1987 using traditional methods, i.e. based solely on its anatomical features. In the case of parasitic nematodes, the key characteristic for distinguishing different species is the shape of the genitalia and tail appendages of the male specimen (such features are too indistinct in the females across different species).

For this particular study, a group of biologist from Portugal and Spain went to the Canary Islands to collect S. atlanticus from Gallotia lizards, as well as sampling for other species of Spauligodon from lizards of southern Spain, Morocco, and Armenia. They compared the DNA sequences of the worms and found that nematodes that had been identified as S. atlanticus (based on their anatomy) actually consisted of two distinct species. While they looked the same, their molecular signature revealed two separate lineages; an eastern lineage that is specific to the lizard species Gallotia atlanticus, and the western lineage that is found in 4 different Gallotia species. They also differ in their evolutionary relationships with other nematodes in the Spauligodon genus. The eastern lineage is more closely related to nematodes in wall lizards (Podacris spp.) from southern Spain and Morocco while the western lineage is more related to worms in green lizards (Lacerta spp.) from Armenia.

These two genetically separate lineages of S. atlanticus are what are known as a cryptic species complex (something that we have previously covered on this blog). Recent studies in the last ten years have shown that some parasite species which had previously been thought to be a single generalist species infecting multiple hosts, are in fact composed of multiple specialised species in disguise.

Meanwhile, this study raises another question - how did these two genetically separate lineages, living in different lizards, evolve such similar anatomical characteristics? The authors of the paper raised the possibility that the anatomy of the two lineages had evolved to convergence due to similar conditions they encounter inside the gut of their respective lizard hosts, or that even sexual selection was responsible, since the key anatomical difference use to distinguish these nematode species is the shape of the male genitalia. But this is a question that will only be resolved with further analyses of related Spauligodon species. As the authors wrote in the title of their paper, there are "no simple answers".

Image from the Wikipedia.

Reference:
Jorge, F., Roca, V., Perera, A., Harris, D.J. and Carretero, A. (2011) A phylogenetic assessment of the colonisation patterns in Spauligodon atlanticus Astasio-Arbiza et al., 1987 (Nematoda: Oxyurida: Pharyngodonidae), a parasite of lizards of the genus Gallotia Boulenger: no simple answer. Systematic Parasitology 80:53-66

Apocephalus borealis

Many of you have heard of the very scary phenomenon called "Colony Collapse Disorder" - and if you haven't, you should, because it could be a major threat to the food we eat. CCD is when the worker honey bees abandon their hives and die, which, if widespread, can mean drastic decreases in pollination of crops. This phenomenon was first reported in the U.S. in 2006 and ever since that time, scientists have struggled to uncover what was responsible. Everything from cell phone radiation to genetically modified crops to a variety of parasites of honey bees were suggested to be the cause. Then, today, a new paper in PLoS One showed data suggesting that another kind of parasite is linked to CCD. Apocephalus borealis is a parasitoid fly that was known to attack bumblebees and paper wasps, but now has been demonstrated to also attack honeybees in the U.S. - in fact, 77% of the colonies sampled near San Francisco were parasitized by A. borealis. The authors used DNA barcoding to confirm that the flies in the honey bees were genetically indistinguishable from those parasitizing bumble bees.

The authors of the new study also found that bees that were found flying around at night (something honey bees don't normally do) were significantly more likely to be parasitized by the fly and furthermore, the sick bees also seemed disoriented. It is not currently known whether or not the tendency for the parasitized bees to fly at night away from their colonies is another example of manipulation of the host by a parasite or whether this might be an act of altruism by the bee, carrying its parasite away from its colony and thus protecting the others.

Although these new results are very exciting, many questions remain to be answered about the history and impact of A. borealis. First, when did the switch into honey bees occur? Honey bees are not native to the U.S., but since they are so well monitored and studied, the authors believe that the switch must have happened recently - otherwise it would have been noticed by apiculturists. Second, could these flies also be serving as vectors for other bee pathogens? Two known bee pathogens, Deformed Wing Virus and Nosema ceranae, a microsporidian were found in the A. borealis flies. And finally, could the invasion of honey bees by this parasite mean that CCD is going to increase? The natural hosts of A. borealis are bumble bees, which live in small colonies where only the queen herself survives the winter, but honey bee colonies have thousands of bees and their activity maintains some amount of heat, even in colder winter months. This increase in host resources and more generations per year could spell a population explosion of A. borealis...and that won't be good for those of us who depend on pollination - like all of us.

The image is from the paper. Look closely at the abdomen of the bee - that's a little parasitic fly laying eggs into it. Soon the larvae will emerge from the dead host. (You can see a photo of this in the original paper as well.)

Source: Core A, Runckel C, Ivers J, Quock C, Siapno T, et al. (2012) A New Threat to Honey Bees, the Parasitic Phorid Fly Apocephalus borealis. PLoS ONE 7(1): e29639. doi:10.1371/journal.pone.0029639.