Acanthocephalus rhinensis

image from figure 1 of the paper

The study which forms the basis of today's post features an acanthocephalan - also known as a thorny-headed worm - which lives in the intestine of European eels in Lake Piediluco in central Italy. Acanthocephalans spend their adult lives like tapeworms, clinging to the wall of their host's intestine, and absorbing nutrients from the pre-digested gut content. But unlike tapeworms, which mostly use suckers and small hooks to cling to the intestinal wall, an acanthocephalan has a formidable bit of armament which puts the tapeworms to shame. As its name indicates, at the front of the acanthocephalan is a hook-laden proboscis (see the picture on the right) to stab into the intestinal wall and firmly anchor themselves in place.

In Lake Piediluco, some eels were found to be infected with up to 350 Acanthocephalus rhinensis, though most eels had fewer than 50 worms. The eels become infected through eating little shrimp-like crustaceans called amphipods. The amphipods live mostly amongst the aquatic vegetation at the edge of the lake, and they are parasitised by the larval stage of A. rhinensis. If you thought the idea of having dozens of prickly-headed worms clinging to your intestinal wall with their nightmarish probosces is bad, A. rhinensis is downright brutal to the amphipod host.

image from figure 3 of the paper

The larval worm (called a cystacanth) occupies a large part of the little crustacean's body (see picture on the left), displacing many of its internal organs. About one in ten amphipods at Lake Piediluco are infected with A. rhinensis, and each amphipod had one or two worms inside them (probably because there wouldn't be much room for more). Acanthocephalus rhinensis imposes a massive burden on the little crustaceans - infected females can only successfully produce half as many eggs as uninfected females.

Armed with that formidable anchor, you would think that A. rhinensis would be able to establish itself in the gut of just about any fish it finds itself in. But it appears to be remarkably faithful to eels, which are the only fish found to have A. rhinensis in their intestines. Perhaps there are other immunological or ecological reasons that prevent this species from successfully infecting other fish.

In addition to establishing the life-cycle of A. rhinesis, another discovery made by the researchers actually served to amend an existing error in the scientific literature. In the original description of A. rhinensis, which was made based on nine specimens, this species is supposed to have a distinctive band of orange-brown (think spray-on tan) pigment just behind their proboscis, a feature that apparently distinguishes it from all the other Acanthocephalus species. However, the researchers who wrote this paper examined a total of over a thousand worms and not a single one had the supposed distinguishing band. But what gave those worms that orange-brown collar? The researchers suggested that this was caused by discolouration from being jammed so deeply into the intestinal wall that the worms inadvertently absorbed pigment from host's intestinal vessel which gave them a distinctive tinge just behind their proboscis.

So in addition to working out the life-cycle of A. rhinensis, this study also served to clarify old mistakes, which will help out any future researchers who work on this species.

Reference:
Dezfuli, B.S., Lui, A., Squerzanti, S., Lorenzoni, M. and Shinn, A.P. (2012) Confirmation of the hosts involved in the life cycle of an acanthocephalan parasite of Anguilla anguilla (L.) from Lake Piediluco and its effect on the reproductive potential of its amphipod intermediate host. Parasitology Research 11: 2137-2143.

Macrodasyceras hirsutum

On this blog, we have featured many parasites that drastically alter the appearance and/or behaviour of their host, usually to make them more likely to be eaten by the next host in the parasite's life-cycle. But today, we are featuring a parasite that makes their hosts appear less appetising - a seed parasitoid that has other plans for its host - none of which involves being eaten.

From the perspective of the plants that produce them, fruits are a way to turn animals into willing seed couriers. By wrapping seeds up in a tasty package, plants can deposit their seeds temporarily inside the body of an animal that will carry them off to a new location. We have even featured a (parasitic of course) plant on this blog that uses beetles for such a purpose.

photo from Figure 1 of the paper

Unlike the rest of the plant, which is often indigestible and laden with defensive toxins, the fruit is supposed to be attractive and appetising to would-be animal dispersers. However seed parasitoids such as Macrodasyceras hirsute have other plans for the fruits - they do not care for the fruit's flesh - they are only after the nutritious seed. Unlike the parasite we featured in the last post, the gullet of a bird is a death sentence for the larvae of this parasitoid (though as always in nature, there are some exceptions), which is a bit of an inconvenience as the fruits it parasitises are meant to be eaten by birds.

Macrodasyceras hirsutum parasitises the fruit of the mochi tree Ilex integra and all it wants to do is to live out its larval stage munching on seeds and grow up to be a wasp. It would rather not have its life suddenly interrupted by a hungry bird feasting on the mochi tree's bright red ripe berries.

So to ensure that its home will not end up tumbling down the throat of a bird, M. hirsutum larvae counteract the berry's usual ripening process, and ensure that it stays green (and unappetising to birds, which disdain unripe berries). A team of Japanese scientists found that if they shielded the fruits from wasp attack, almost all the mochi berries ripened to red. But, if they are exposed to M. hirsutum, some of them stayed green, and all the berries that stayed green had M. hirsutum larvae living inside them. Furthermore, they found that the more larvae there are in the berry, the more intensely green the fruit becomes - M. hirsutum did not merely stop the berries turning from green to red, they actually turned the dial on the green tone all the way up.

This little wasp is not the only insect to do this. Holly berries infected with a species of midge also stay green. It is unknown how this wasp interferes with the berry's pigment production/development, though for the holly berry midge it has been suggested that a symbiotic fungi is responsible for maintaining the host fruit's green colour. The relationship between fruit-bearing plants and fruit-eating animals has evolved to be a mutually beneficial interaction whereby one party provides food (fruits) while the other returns with a service (seed dispersal). But, the actions of M. hirsutum and other such seed parasitoids tinkering away in the background can certainly undermine the effectiveness of this mutualistic partnership if they cause otherwise ripened fruits to go uneaten. The extent of the impact such seed parasitoids have on the ecology and evolution of such plant-animal interaction is currently unknown.

Reference:
Takagi, E., Iguchi, K., Suzuki, M. and Togashi, K. (2012) A seed parasitoid wasp prevents berries from changing their colour, reducing their attractiveness to frugivorous birds. Ecological Entomology 37: 99-107.

Philophthalmus sp.

We have featured many parasitic flukes on this blog, and a part of their life-cycle consists of the free-living stage (called a cercaria) being expelled from its mollusc host (where they are produced asexually), and proceeding to infect the next host. There, they form a cyst and wait to be eaten by the final host. But today's parasite, also a fluke, does something slightly different. Unlike most other trematodes that penetrate and embed themselves inside the host's body, Philophthalmus attaches itself to hard surfaces, which just so happen to be objects that are likely to be swallowed by shorebirds - such as the surface of a shellfish. From my personal experience, this tendency also made them a bit of a nuisance in the lab as they tended to stick to pipette tips and the bottom of plastic petri dishes and had to be scraped off (see the accompanying photo).

Not all of the objects that are available for attachment by Philophthalmus would necessarily end up going down the gullet of a bird, however. There is an abundance of small rocks and seaweed in the intertidal environment where Philophthalmus is found - but those are not the usual fare of shorebirds that prefer a more appetising diet of seafood like snails and crabs. A pair of scientists from University of Otago set out to see if Philophthalmus shows preferences for certain types of substrates. First, they surveyed and calculated the exposed surface area of various objects on the mudflats (such as snails, crabs, seaweed, rocks, etc), then estimated the number of Philophthalmus cysts that would be expected to be attached to each of them if the cercariae just distributed themselves evenly across the environment and stuck to whatever they come across first. They also did a series of laboratory experiments to test if Philophthalmus cercariae show any preference for specific types of objects.

They found that instead of attaching themselves to whatever that just happened to be laying around, there were a higher number of Philophthalmus cysts on snails than expected given their comparatively small surface area. This makes sense in terms of the parasite's life-cycle as the shell of a live snail is more likely to deliver Philophthalmus to the mouth of a bird than say, bits of rock and seaweed. Additionally, in laboratory experiments, when Philophthalmus cercariae were presented with the type of substrate usually present on the mudflats, they showed a very high tendency to stick themselves to snails, but shunned rocks and the shells of cockles.

So why the preference for snails but not cockle shells? Some birds do eat cockles and for some parasites that is how they complete their life-cycle, but when birds such as the oystercatcher eats a cockle, they usually crack open the valves to swallow the flesh (where the parasites are embedded), leaving the shell behind. Snails, however, are more likely to be eaten whole (with the attached Philophthalmus cysts). Oddly enough, the Otago scientists found very few cysts attached to crabs - which is another staple food for birds. However, a crab tends to go through several molts during its life, and every time it does so, it would leave behind any Philophthalmus cysts which are attached to its carapace, and birds don't usually go around picking up empty crab shells to eat.

It is worth pointing out that it would be equally useless for Philophthalmus to attach itself to the shell of a dead snail. Therefore, it is possible that these cercariae are able to detect chemical cues that allow them to distinguish between dead and live snails. Other cercariae are known to be able to respond to a wide range of stimuli, and there no reason to think that Philophthalmus would be all that different - perhaps that would be the next stage of research into this species...so watch this space (or species as the case may be)...

Reference:
Neal, A.T., and R. Poulin. 2012. Substratum preference of Philophthalmus sp. cercariae for cyst formation under natural and experimental conditions. Journal of Parasitology 98: 293-298

Cuscuta chinensis

Today's post has some plant-on-plant action, featuring a species of dodder. Dodders are a group of holoparasitic plants made up of about 100-170 species. They are plants that consistent entirely of stem, with leaves that have been reduced to tiny scales. They smother the host plant in a tangled mess, and dig deep into the host tissue using modified roots called haustoria to draw out water and nutrients. We have previously featured the European Dodder on this blog, but today, we will be looking at the Chinese Dodder Cuscuta chinensis, and how it interacts with plants that are not native to its home range.

Image Credit: Jayesh Patil

There are many studies that look at characteristics of successful invasive species (an introduced species that has subsequently become a pest). Generally, plants that have become invasive after their introduction have faster growth rates and are able to utilise nutrients more efficiently, allowing them to outcompete the native flora. In addition, according to the "enemy release" hypothesis, one of the reasons why newly introduced plants and animals become so successful in their new homes is because they are freed from the burden of their natural predators and pestilence, thus allowing them to propagate unchecked across the new land. While this seems to indicate that the best way to control invasive species is to introduce their natural enemies as well, the main problem is that you are introducing yet another new species. Remember that folklore about the old lady who swallowed a fly and subsequently introduced a sequential menagerie into her body? You don't really know what cascading effects the new biological control species will have on the local ecosystem - after all, the cane toad (Bufo/Rhinella marinus) was introduced to Australia to control beetles in sugar cane plantations, but have since become a huge ecological problem.

The higher growth rate and resource-usage efficiency of these invasive plant does have a drawback though - it makes them more attractive targets to parasites. So what if a native parasite can turn the table on the invaders? What if a native parasite acquires a taste for an exotic new host?

The Chinese Dodder is a parasite with eclectic tastes, as it is capable of infecting more than 100 species of wild and cultivated plant species. To find out how well C. chinensis grows on native flora compared to their introduced counterparts, a team of researchers in China evaluated the performance of C. chinesis on 3 invasive plant species and the native equivalent from the same genus. They found that not only did C. chinensis grow much more prolifically on the introduced plants,but it also caused more damage. In fact, C chinensis is more damaging to plants that are more efficient in using their resources - the very trait which makes them so good at being invasive in the first place.

There is also another possibility - one which the researchers did not mention in the paper: Unlike the native plants which have had a long co-evolution history with the dodder and have thus evolved various means to counter the parasite's tricks blow-by-blow, the naive introduced species have never encountered C. chinesis before, which leaves them more vulnerable to attacks by the parasitic dodder. For those exotic introduced plants, it seems that the very thing which had brought them so much success in their new home may end up causing their downfall when confronted with a certain holoparasite.

Reference:
Li J, Jin Z, Song W (2012) Do Native Parasitic Plants Cause More Damage to Exotic Invasive Hosts Than Native Non-Invasive Hosts? An Implication for Biocontrol. PLoS ONE 7(4): e34577. doi:10.1371/journal.pone.0034577

Paragordius obamai

Sex is one of the great mysteries of evolutionary biology - why do organisms have it? It has numerous costs associated with it, including the two big ones, which are that only half the population will produce offspring in the next generation (technically really a problem more of anisogamy than sex, per se) and that successful gene combinations can be broken up via recombination. There are other costs as well. For instance, finding and wooing mates can be costly to an organism.

Nematomorphs, sometimes called hairworms, are parasites that live inside arthropods as larvae, but then exist as free-living aquatic adults. They often induce suicide in their insect hosts, by causing them to jump into water, where the worms then escape (see this previous post for another example). The adults typically seek out the opposite sex and can form "Gordian knots" of mating worms. Today's species, however, is found in larger and faster-moving waters - and in these big, complicated habitats, finding a suitable mate can be really tricky. So, today's parasite, has solved this problem through the evolution of parthenogenesis. Meet Paragordius obamai, (named after President Obama, in honor of it being discovered in Kenya, where his father was raised), a species of nematomorph that has completely given up on males. When brought into the lab, P. obamai only released female worms and nowhere inside these stringy parasites could male reproductive organs be found. Because bacterial symbionts can sometimes produce severe sex-ratio biases or even male-killing in insects and other invertebrates, the authors used pyrosequencing to look for evidence of these micro-manipulators, yet found no sequences similar to the taxa that have been observed to cause these biases in other hosts.

The authors now plan to use this new species, in comparison with a sexual congener, to test hypotheses on the evolution of and genetic mechanisms responsible for this novel parthenogenetic situation.

Source: Hanelt B, Bolek MG, Schmidt-Rhaesa A (2012) Going Solo: Discovery of the First Parthenogenetic Gordiid (Nematomorpha: Gordiida). PLoS ONE 7(4): e34472. doi:10.1371/journal.pone.0034472

Image from the paper.

Contributed by Susan Perkins.

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