Stylops ater

Strepisptera is an order of parasitic insects with some very unique characteristics.They are also known as twisted wing parasites, based on the twisted hindwings on the male parasite. They infect many different orders of insects, but mostly target wasps and bees where they up take up residency in the host's abdomen. If you know what to look for, you can immediately spot their presence. In fact, there's even a special term for describing bees and wasps that are parasitised - they get "stylopized".

Top: A male Stylops ater (indicated by red arrow) attempting to mate with a female in a bee's abdomen.
Bottom left: Female Stylops ater adult (indicated by red arrow) in a bee's abdomen,
Bottom right: Male Stylops ater pupa casing (indicated by red arrow) in a bee's abdomen. 
From Fig. 1 of the paper

And it's not just the hindwings of stresipterans that are a bit twisted, these insects have extreme sexual dimorphism, so much so that if you didn't know any better, you'd think the females and males are completely different types of animals. The female stresipteran looks like a grub, and she spends her entire life inside the abdomen of the host, with just her head partially poking out from between the segments of the host's abdomen.

In contrast, the males have a pair of giant compound eyes, prominent branched antennae and the "twisted wings" that give this group of insects its name. They have a short and frantic adulthood - after emerging from the host, he only lives for a few hours and his sole mission in life is to find and mate with an elusive female strepisteran, hidden away in the abdomen of a host insect. And he does the deed with an appendage that entomologist Tom Houslay once vividly called a "stabby cock dagger". The technical term for this form of mating is "hypodermic insemination" - where the male basically stabs and inject his sperm into the female, and the sperm somehow find their way to the eggs. Strespiterans are not alone in having this type of appendage, male bed bugs also have a stabby cock dagger - but that's another story.

The study being featured in this post focuses on Stylops ater, a species which parasitises Andrena vaga, the grey-backed mining bee. Unlike the honeybees that most people are familiar with, these are solitary bees, with no castes. And while they do gather into an aggregation to nest, each bee just builds and looks after their own nest. The researchers examined a population of these bees in Lower Saxony, Germany. They sampled over two periods, during late winter, when all 508 bees they looked at were stylopized, and late spring, when they only managed to find two stylopized bees out of a total of 150.

Almost two-third of the stylopized bees were female, but these parasites seem to prefer hosts that are of the same sex as themselves. Since female bees live longer and can provide more nutrients than male bees, this works out well for the life history of female Stylops as it gives them more time and nutrients to grow her brood. After mating, the female Stylops can release up to 7000 offspring, which crawl off to find other bees. While each larva is merely 0.2 millimetre long, they can traverse long distances by hitching a ride on the hair, pollen sacks, or even the crop of bees, to end up in a new bee nest, filled with fresh hosts.

While most bees only hosted a single parasite, some had two or three, and the researchers did find one very unlucky bee that was harbouring four Stylops in its abdomen. But even a single Stylops can take a severe toll on its host. In fact, this parasite is so demanding that it wouldn't grow as big if it had to share its host with another Stylops. As a result, bees infected with Stylops are unable to develop eggs or only produce poorly developed eggs.

But aside from effectively sterilising the bee, Stylops also tinkers its host's biological clock, making it emerge out of hibernation a few weeks earlier than uninfected bees - hence why the researchers found so many stylopized bees in late winter. Making the bees such early risers ensures that there will be plenty of female Stylops around for the male Stylops to find, which will be emerging at that time to live out their extremely short lives. It also gives the female Stylops' larvae more time to develop, so they will be able to crawl off in time to find new hosts in the bee's brood cells. This type of behaviour manipulation is comparable to what's found in Sphaerularia vespae, a nematode that alters the seasonal biological clock of hornet queens.

In order to make these changes to the bee's internal clock, Stylops would have to manipulate the host's hormones, but this also results in some side effects on the bee's body. Female bees that get stylopized tend to have a hairier back, skinnier legs, and the hairs on said legs become shorter and more sparse. In short, they take on characteristics that are more similar to that of regular male bees.

So next time you are out and about, keep an eye out for a bee that looks a bit different from the rest. It might be flying under the influence of a parasite tucked away in its abdomen, looking to make a rendezvous with her short-lived partner.

Reference:

Hoffmann, M., Gardein, H., Greil, H., & Erler, S. (2023). Anatomical, phenological and genetic aspects of the host–parasite relationship between Andrena vaga (Hymenoptera) and Stylops ater (Strepsiptera). Parasitology 150: 744-753

Atriophallophorus winterbourni

In Lake Alexandrina of New Zealand lives a species of tiny freshwater snail called Potamopyrgus antipodarum. These snails are capable of alternating between sexual and asexual reproduction and can be extremely abundant. So much so that they have become invasive in many other parts of the world. Outside of their original home, they are free to proliferate to their heart's content. But back in New Zealand, these snails don't always have things go their way. They are held back by a whole menagerie of flukes which parasitise them - at least 20 different species in fact.

Top: Photo of the snail Potamopyrgus antipodarum by Michal Maňas, used under Creative Commons (CC BY-SA 4.0) license. Bottom: The metacercariae cysts of Atriophallophorus winterbourni, from Figure 1 of the paper.

These flukes have a range of different life cycles, but all of them use P. antipodarum as a site of asexual reproduction - converting the snail's insides into a clone factory and rendering it sterile in the process. These flukes might be the reason why these snails continue to engage in sex every now and then, despite asexual reproduction being much more efficient. Sex is necessary to maintain genetic variations - the key ingredient in the evolutionary arms race against all those flukes.

Researchers who have been studying these snails and their flukes noticed that while all 20 species of those parasite are essentially body snatchers that take over the insides of their unwitting host, one species - Atriophallophorus winterbourni - goes beyond simply messing with their host's physiology and seems to be influencing the snail's behaviour too. Snails infected with A. winterbourni tend to be found in the shallow areas of the lake. Among snails collected from the shallow water margin of the lake, they represent 95% of the infections. Is this because those areas just happen to be hot spots for snails to get infected with A. winterbourni? Or are these flukes actually coaxing the snails into hanging out in the shallows?

To figure out if there's something special about A. winterbourni, researchers compared snails infected with A. winterbourni with those that were infected with a different species of fluke - Notocotylus - to see if such behavioural change is simply a side-effect of fluke infection, or if it is something specific to A. winterbourni. The researchers did this by setting up a series of ten 5 metres long tubular mesh cages that stretched across different depth clines in the lake, from less than 0.8 metres at the shallow end to 2.8 metres at the deep end, with different sections of the cage corresponding to different levels of water depth. Using snails collected from two high infection prevalence sites at the lake, they added about 800 snails to the deepest section of each cage, and the snails were allowed to freely roam between the different sections. After eleven days, samples of snails were randomly collected from each depth level and examined for parasites.

There are some key differences in the life cycles of A. winterbourni and Notocotylus that makes them good for comparisons. Just like other flukes, A. winterbourni undergoes asexual reproduction inside the snail host, producing a whole load of clonal larvae. But unlike many other flukes, these clonal larvae stay in the snail and transform into cysts, where they wait to be eaten by a duck hungry for snails. In contrast, snails that are infected with Notocotylus release those clonal larvae into the surrounding waters, and they do so continuously over the course of about 8 months. These larvae attach themselves to vegetation or the shells of other snails, and are transmitted to grazing ducks that accidentally ingest them. Therefore, unlike A. winterbourni, their transmission is largely decoupled from the snail's own movement and behaviour.

So after those eleven days of allowing infected snails to roam in the cages, what did the researchers find? Well, snails infected with A. winterbourni were heavily distributed towards the shallow end, with over a third of the snails in that section being infected, which is over three times higher than the expected background infection level (11%). In the deepest section of the cage, A. winterbourni-infected snails were rare, representing only 3-5% of the snails in that section, and some of them were immature infections. In contrast, those infected with Notocotylus were found to have distributed themselves fairly evenly across the entire depth cline. It is unclear what exactly A. winterbourni is doing to the snails that makes them favour shallow water, but more importantly, why would they do this? What's in it for the fluke? Well, the final hosts for A. winterbourni are dabbling ducks that only feed in the shallow parts of the lake. So in order for A. winterbourni to make a successful rendezvous with its final host and complete its life cycle, it will have to prod its snail host into the shallows.

Atriophallophorus winterbourni belong to a family of flukes called Microphallidae, and there are a few other species in this family which are also known host manipulators. For example, Gynaecotyla adunca is a species that infects marine mudsnails, and it coaxes its mudsnail host into stranding itself onto beaches, which brings them closer to the crustaceans that serve as the next host in the parasite's life cycle. There's also Microphallus papillorobustus, which infects little sand shrimps (amphipods), and it alters their behaviour in a number of different ways that makes them more visible to hungry birds. Even though not all members of Microphallidae are host manipulators, it's a trait that does seem pretty common in this fluke family. Sometimes, in order to complete a life cycle, you just have to drag that snail to where you need it to be.

Reference:

Feijen, F., Buser, C., Klappert, K., & Jokela, J. (2023). Parasite infection and the movement of the aquatic snail Potamopyrgus antipodarum along a depth cline. Ecology and Evolution 13: e10124.

Hymenoepimecis bicolor

Over the course of human history, numerous species of plants, animals, and other organisms have been taken from their original habitats and introduced (either intentionally or accidentally) to other parts of the world. Some of those introduced species become "invasives" in their new home, partly due to the lack of natural enemies. But while many invasive species get a brief moment of respite from their old adversaries, the local parasite and predators quickly catch on that the new arrival could be added to their menus too. This was the case for a species of spider that has been introduced to Brazil, where it ended up attracting the attention of a mind-controlling wasp.

Left top: Hymenoepimecis bicolor larva on a spider host, Left bottom: Developing H. bicolor cocoon in a cocoon web,
Right: an adult H. bicolor wasp.
Photo of H. bicolor larva from Fig. 2 of this paper, Photos of cocoon and adult H. bicolor from Fig. 7 and 9 of this paper

Hymenoepimecis bicolor is a species of parasitoid wasp that belongs to a subfamily of wasps called Pimplinae. All the members of that subfamily are a spider's worst nightmares. These wasps specialise in attacking spiders at every stage of their lives - some species go after the unhatched eggs in silk sacs, while others tackle fully-grown adult spiders. Not only that, some of them are also masterful mind manipulators that induce their host spider into spinning a special web called a "cocoon web" that secures the wasp's developing cocoon. And Hymenoepimecis bicolor just happens to be one such manipulator.

Among the pimpline wasps, each species have their own host preferences and in the case of H. bicolor, one of its usual hosts is the golden silk orb-weaver (Trichonephila clavipes), a spider which is native to Brazil. When a female H. bicolor spots a potential host, she flies in and grapples with it, immobilising the spider by stabbing it in the mouth with her ovipositor, before checking it for other wasp eggs, and then planting one of her own. The thing about the golden silk orb-weaver is that while the juvenile spiders are relatively easy for H. bicolor to handle, once the spiders reach adulthood, they become more dangerous for the wasp to tackle. 

Nevertheless, limited host availability means that the wasp sometimes need to go after the bigger spiders anyway, with demand being so high that some spiders end up being parasitised by two wasp larvae at the same time. But the arrival of the tropical tent-web spider (Cyrtophora citricola) has provided H. bicolor with some new options.

The tropical tent-web spider has spread to many parts of the world by hitchhiking in shipments of fruit, potted plants, or packing material, and it has made its way to South America about three decades ago. And it just so happens that their size and habits place them firmly in the sight of H. bicolor. Not only is the tent-web spider in the preferred size range for H. bicolor to parasitise, much like the native orb-weavers, this introduced spider constructs open webs that leave them exposed to attacks. Researchers found that the H. bicolor larvae are able to successfully parasitise the tent-web spider just as well as the native spiders.

While H. bicolor larvae grow well and pupate as usual on the tent-web spiders, it seems that they haven't yet achieved complete mastery over this new-fangled host. As mentioned earlier, when these wasps are ready to pupate, they commandeer their spider hosts to weave a special "cocoon web" that suspends the developing wasp cocoon in mid-air. This makes the cocoon less accessible to any would-be predators or hyperparasitoids. Hymenoepimecis  bicolor embellish that with an added layer of security, by inducing the spider to also build a series "barrier threads" around the cocoon that further bar entry, as well as making the web more stable

This is where the introduced spider host falls short. While the parasitised tent-web spider is able to produce the usual cocoon web with the necessary structure to support and suspend the developing cocoon, it lacks the finishing touches of those additional barrier threads. Ironically, compared with the spiders that H. bicolor usually targets, the regular webs made by the tent-web spider actually needs less modification to make it suitable for the wasp's cocoon.

Based on what's known about these wasps, when it is ready to pupate, the wasp larva produces a cocktail of chemicals that place the spider under its spell. But in this case, it looks like that cocktail formula needs a bit of tweaking to work its full magic on the introduced tent-web spider. While not perfect, it serves its purpose well enough, and the introduction of this spider has allowed a parasitoid wasp to expand its host horizons.

Reference:

Gonzaga, M. O., Pádua, D. G., & Quero, A. (2022). Inclusion of an alien species in the host range of the Neotropical parasitoid Hymenoepimecis bicolor (Brullé, 1846)(Hymenoptera, Ichneumonidae). Journal of Hymenoptera Research 89: 9-18.

Polypipapiliotrema stenometra

Corals are host to a wide range of pathogens and one of the most unusual is a type of parasitic fluke which cause the polyps of Porite corals to become pink and puffy. Parasitic flukes (trematodes) have complex life cycles and are known to use a wide variety of different animals as temporary hosts in order to complete their life cycles. The fluke larvae that infect coral polyps complete their life cycle in coral-eating butterfly fishes, and their existence have been known for decades.

Left: taxonomic drawing of an adult Polypipapiliotrema stenometra from Fig. 2 of the paper.
Right: Pink, swollen Porites coral polyps infected with Polypipapiliotrema larvae (photo by Greta Aeby).

For quite a while, they were considered to be just another species within a genus call Podocotyloides, specifically Podocotyloides stenometra. But a recent study by a group of researchers found that not only are these coral-infecting flukes distinctive enough to be placed into its own genus called Polypipalliotrema, but that the flukes which have previously been classified collectively as "Podocotyloides stenometra" is in fact a whole conglomerate of different species, infecting coral polyps far and wide.

In this study, researchers examined 26 species of butterfly fishes collected from the French Polynesian Islands, and O'ahu, Hawai'i, and found 10 species which were infected with Polypipaliliotrema. Upon examining the DNA and the physical features of those flukes, they discovered that what was thought to be a single species turns out to be at least FIVE different species of coral-infected flukes, and there are variations in their geographical distribution.

Butterfly fish species that are found across different locations were sometimes found to have different species of Polypipapiliotrema at each location, so it seems some fluke species were localised to particular island groups. This means there might be more unique species of coral-infected flukes that remain undiscovered and undescribed from other coral reefs around the world.

In order for Polypipalliotrema to complete its life cycle, it needs the host polyp to be eaten by a butterfly fish. While coral polyps are stable food for some fish, they can be small and finicky to handle - you have to be quick and precise in picking the coral polyp lest it retreats back into its skeleton. Also, corals usually occur in vast colonies composing of hundreds and thousands of polyps, so the chances that the infected polyp would be among the ones eaten by a butterfly fish would be quite slim. On top of that, the polyps of Porite is consider to be poor quality food for most coral-eating fishes - their polyps are tiny and quick to retracts into its skeleton - so even fish that feed almost exclusively on coral polyps prefer species other than Porites.

But Polypipalliotrema has a clever way of stacking the odds in its favour, and it does what many parasites do - by manipulating its host. Coral polyps infected with Polypipalliotrema become swollen and bright pink, in complete contrast to the tiny uninfected polyps. Not only does the colouration draws the attention of butterfly fish, the swollen polyp also can't retract into the coral skeleton, making it easier to the butterfly fish pick them up and get more coral flesh for every mouthful.

But why should the butterfly fish eat something that is filled with parasites? Shouldn't they try to avoid parasitised prey, especially when the infected polyps are so easy to distinguish? Since this fluke is commonly found in butterfly fish, it is clear that they make no attempt at avoiding the fluke-laden polpys.

This could be that while Polypipapiliotrema is technically a parasite, it doesn't really harm the fish host that much, and because of what the fluke larvae do to coral polyps, the fish have an easier time getting its meal. As such, the relationship between Polypipapiliotrema and butterfly fishes is closer to a form of mutualism - by altering the coral polyp, the fluke helps butterfly fish get more to eat for less effort, and for its side of the bargain, butterfly fish allows the fluke to complete its life cycle.

Reference:
Martin, S. B., Sasal, P., Cutmore, S. C., Ward, S., Aeby, G. S., & Cribb, T. H. (2018). Intermediate host switches drive diversification among the largest trematode family: evidence from the Polypipapiliotrematinae n. subf.(Opecoelidae), parasites transmitted to butterflyfishes via predation of coral polyps. International Journal for Parasitology 48: 1107-1126.

Dicroceolium dendriticum (revisited)

The lancet fluke (Dicroceolium dendriticum) is one of the most well-known and oft-cited example of parasite host manipulation. But in most people's mind, it often gets mixed up with the Cordyceps zombie ant fungus, which is understandable given that they both (1) manipulate an ant's behaviour, and (2) makes it climb onto vegetation. But that's where the similarities ends.

The lancet fluke and the zombie ant fungus are very different organisms, with very different plans for their ant host. First of all, the lancet fluke is a a type of parasitic flatworm which infects three different host animals throughout its life cycle - unlike the fungus which only infect the ant. And whereas the zombie ant fungus kills its host once it has reached the desire location to disperse its spore, the lancet fluke's endgame is to use ant as a way of reaching a mammal's belly, and it will make the ant repeat the climbing routine until that is accomplished.

Top: Internal structure of a lancet fluke-infected ant. Bottom: Internal structure of an (A) infected and (B) uninfected ant's head. Labels: emc (encysted metacercaria), nmc (nonencysted metacercaria), oe (), sog (suboesophageal ganglion)
Images from Figure 2 and 3 of the paper

In order to understand why lancet fluke does what it does to ants, let's look at its life cycle. The adult fluke lives in the bile duct of herbivorous hoofed mammals such as cattle, sheep, and deer. The adult fluke can produce hundreds or even thousands of eggs per day. These eggs are release into the outside world with the host's faeces, and some of them are swallowed by land snails.

The parasite turns the snail into a biological factory that churns a clone army of fluke larvae, which are packaged by the dozens into slime balls. These slime balls ooze out of the the snail's body, and are gobbled up by ants which find them to be an irresistible delicacy. Inside the ant, the parasite turns into what's known as a metacercaria and waits to be eaten by the final host. Given the final hosts of the lancet fluke are grazing mammals - none of which are particularly fond of eating ants - how is this parasite supposed to complete its life cycle? The lancet fluke solves this problem by making the infected ant climb onto and clamps itself to a bit of vegetation that such herbivores would eat, such as a blade of grass or a flower.

Unlike the zombie ant fungus where the ant stays locked in place and perishes once it has been moved into position, the lancet fluke will adjust the ant's behaviour depending on circumstances. If the surrounding temperature gets above 20ºC (68ºF), the parasite's spell wears off and the ant goes back to acting normal, since a hot sun-baked host is also bad for the parasites inside it. Once the temperature drops, the ant goes back to being in the parasite's thrall. While this striking example of host manipulation is well-known, exactly how the lancet fluke does that is a bit of a mystery.

The development of X-ray micro-computed-tomography, also known as microCT, has enable scientists to peer into the interior structure of many organisms, allowing them to, in a sense, perform a "virtual" dissection without inadvertently disrupting or displace the internal structures as a part of the dissection process. I've previously written a blog post about scientists who used microCT to visualise the root network of a body-snatcher barnacle, in this study another group of researchers applied the same technique to look at the lancet fluke in its ant hosts.

The researchers collected some ants from Cypress Hill Interprovincial Park in Canada, at a site which is known to be home to the lancet fluke. When the looked at the internal structure of the infected ants using microCT, they found that the parasites distribute themselves throughout the ant's body in a very specific way. When an ant eats a slime ball, it swallows a batch of genetically identical parasite clones, most of which will take up resident in the ant's gaster (its abdomen) and become "encysted" - curled up and wrapped in a protective membrane. But no matter how many lancet flukes the ant ends up with, there is always one unencysted larva which is embedded in the ant's head - specifically underneath its suboesophageal ganglion (SOG).

The SOG can be considered the cockpit of an ant - it is a control hub responsible for regulating the ant's behavioural patterns. Unlike its clonal sibs which are wrapped up in a cyst and walled off from the outside, this "head fluke" can continue to interact with and push the ant's neurological buttons from the SOG. Exactly what kind of physiological exchange is taking place between the parasite and the ant's brain has not been determined at this point, but it seems pretty clear that this "head fluke" plays an important role.

But being able to control the host come at a significant cost for the fluke. Unlike its clone mates which are enclosed in a protective coat, the "head fluke" has to sit naked and exposed because it needs to interact with the ant's brain. The cyst wall is what allows larval lancet flukes to survive passing through the final host's digestive system, and the exposed unencysted manipulator parasite will not survive this journey. So in order to bring an ant to a grazing mammal, one little lancet fluke sacrifices itself so that its clone mates will have a prosperous and productive future.

Reference:
Martín-Vega, D., Garbout, A., Ahmed, F., Wicklein, M., Goater, C. P., Colwell, D. D., & Hall, M. J. (2018). 3D virtual histology at the host/parasite interface: visualisation of the master manipulator, Dicrocoelium dendriticum, in the brain of its ant host. Scientific Reports 8(1): 8587.

Massospora cicadina

Periodical cicadas spend most of their lives as juveniles (also known as nymphs), living underground and sucking juices from tree roots. Depending on the species, they keep to this subterranean existence for 13 or 17 years before finally emerging into daylight. And they do so simultaneously in massive numbers. These newly emerged nymphs will climb on to a nearby tree to moult into winged adults. The life of an adult cicada is short and over in about a month. During this period they sing their hearts out and mate until they drop to produce the next generation of cicada nymphs which will return to the soil. But the cicadas aren't the only ones to get busy during this period. Scattered across the landscape are the spores of Massospora cicadina, and for over a decade they have been waiting patiently for the cicadas' return.

Cicadas with and without Masspora infection, note uninfected male cicada which still has the genitalia of an infected female cicada attached. Photos from Figure 1 and 2 of the paper

Massospora cicadina is a parasitic fungus that targets all seven known species of periodical cicadas, and its effects on the host are devastating. Once infected, the cicada is done for - the fungal infection turns the cicada's abdomen into a chalky mass of spores. Surprisingly, despite missing a big chunk of itself, an infected cicada carries on as if it is business as usual - these diseased cicadas keep flying, singing and mating like their uninfected counterparts. But surely there must be more going on beneath that exterior of surprising normality.

A group of researchers investigated if Massospora is doing more to cicadas than just robbing their booties. In particular, they were interested in whether Massospora is altering the cicada's behaviour, as many other insect-infecting fungi are known to do. Since the mid-1990s, they have been spending hundreds of hours documenting the behaviour of both infected and uninfected cicadas. They also collected some of those cicadas and kept them in captivity for closer observations, and played recordings of male cicada songs to them to see how they responded.

There are two ways that cicadas can get infected with Massospora, and how they do so determines what kind of infection they end up with. If a cicada brushed up against some Massospora spores while emerging as a nymph, they end up with what's called a Stage I infection. However, if they picked up the fungus by coming into contact with an infected adult cicada, they would end up with a Stage II infection. Both are equally bad for the cicada, but there are some key differences between them.

Cicadas with Stage I infection tend to crawl around a lot more and leave behind a trail of contagious spores wherever they go. In contrast, those with Stage II infection fly around more often. But aside from that there are also other key behavioural differences, and it relates to what all these cicadas have emerged for - mating. Male cicadas with Stage I infection respond to mating calls the way that female cicadas usually do - with wings flicks that are the cicada's equivalent of "Hey, I'm interested - come and get me!" Any amorous cicadas that respond to this gesture and mate with the infected male also end up contracting the deadly fungus. However those with Stage II infections simply ignored those calls and kept to themselves.

This behavioural change in the infected cicada is more sophisticated that simply turning the male cicada to a "female phenotype". Aside from responding to calls with wing flicks, these male cicadas still behave like other males. The fungus merely added another behavioural response to their repertoire. So what about those with Stage II infection? Why don't they get in on the action?

The spores produced by Stage I infections immediately contagious, so it spreads through the cicada population through physical contact (such as mating). Meanwhile, Stage II infections produce a different type of spores that cannot infect cicadas right away, but can stay dormant and viable in the soil for decades. These spores lie in wait for a future brood of cicadas to emerge, infecting the nymphs as they crawl out of the soil.

In this case, the fungus doesn't need the host to be flirty and rub carapace with other cicadas, they just need it to be a diligent little crop-duster that sprinkle fungal spores all over the landscape. By doing so, Massospora is well-prepared for the next emergence event, when the festival of frantic cicadas and fungal booty-snatchers can start all over again.

Cooley, J. R., Marshall, D. C., & Hill, K. B. (2018). A specialized fungal parasite (Massospora cicadina) hijacks the sexual signals of periodical cicadas (Hemiptera: Cicadidae: Magicicada). Scientific Reports 8(1), 1432.

Glyptapanteles sp.

Today we're featuring a guest post by Niamh Dalton - a student from 4th year class of the Applied Freshwater and Marine Biology' degree programme at the Galway-Mayo Institute of Technology in Ireland. This class is being taught by lecturer Dr. Katie O’Dwyer, who has previous written guest posts about salp-riding crustaceans and ladybird STI on this blog. This post was written as an assignment on writing a blog post about a parasite, and has been selected to appear as a guest post for this blog. Anyway, I'll let Niamh take it from here.

Wasps in adult form are terrifying, right? Humans automatically associate the sight of wasps with sudden panic in the fear of getting a minor sting. What do we really have to be afraid of? After briefly studying the life-cycle of a species of wasp, Glyptapanteles, I assure you it’s not adult wasps we should be frantically sprinting away from, it’s their babies.

Glyptapanteles cocoon being watched over by their caterpillar guardian, from Fig. 1 of the paper

Glyptapanteles wasps are parasitoids, a group of parasites that inevitably kill their host.  Adult females, after mating, will inject their eggs into a live caterpillar. The caterpillar will act as a surrogate womb, giving the eggs a chance to develop into mature larvae as they feed of its bodily fluids. The larvae eventually break through the skin of the caterpillar to complete pupation, meanwhile the caterpillar is still living and undergoes mind control by the parasite, becoming a modified bodyguard and surrogate parent until the larvae break out and fly away, leaving the caterpillar to die of starvation.

As spine chilling as this process is, a team of scientists were particularly interested in this survival technique and they constructed an experiment to investigate the behaviour modifications inflicted by the parasite on their host.

It all begins with a female wasp injecting approximately 80 eggs into the body cavity of a caterpillar using an ovipositor or egg layer. Each egg hatches into a larva in the the caterpillar’s body, feeding only off the bodily fluids and being careful not to damage any internal organs in order to keep the host alive and functional. According to the scientists' observations, there is no behavioural modifications of the host during this internal parasitism stage, however, each larva is the size of a rice grain and the density of the larvae in a caterpillar can have morphological alterations. The caterpillar will grow in girth but not in length, looking ready to explode.

It gets worse. Eventually the larvae have to leave the nest, so to speak. To complete the final stage of maturity, all 80 larvae evacuate the host simultaneously by using their newly developed jagged jaws to slice through the caterpillars’ tough skin. Whilst emerging through the tough material, the larvae release a chemical which only paralyses the host, meaning the host is alive throughout this excruciating process. In order for the larvae to keep their host alive, they coincide their last moulting stage with their exit, filling the holes they have excavated with a ‘plug’ made of their sloughed exoskeleton.

Why would the Glyptapanteles larvae have to keep the host alive after emergence? Well, following their exit, the larvae begin to spin silk strings and form cocoons for their last stage of maturity. At this stage, the larvae are vulnerable to predators and other parasitoid wasp species that can inject their eggs into these larvae (ironically). The host develops behavioural modifications during the parasites pupae (cocoon) stage, acting as a bodyguard. As caterpillars are themselves larvae of butterfly and moths, they too construct a cocoon in their life-cycle. As the scientists found, the host caterpillar will use their own silk string to weave a blanket over the Glyptapantele cocoons for further protection.

That’s not all. The host will increase its number of violent head swings in attempt to scare off any form of disturbance. The host is also known to stand on two pairs of back legs in vigilance and spending a substantial amount time bent over the cocoon mound. In the experiments, the research team found an increase in aggression in caterpillars that were infected with the parasitoids compared in caterpillars that were not exposed to parasites.

The main question that remains was: How is there behavioural modifications in the host after the exit of the parasite? After the dissection of previously parasite-stricken caterpillars, there were 1 or 2 active parasitoids found still in the body cavity. The authors of this paper hypothesised that these leftover larvae are responsible for the mind controlling of the host after emergence. In this way, the parasites sacrifice a few individuals for the survival of the majority of the larvae. This is a uniquely evolved survival technique that is obviously very effective and bitter-sweet in a strange way.

Reference
Grosman, A., Janssen, A., de Brito, E., Cordeiro, E., Colares, F., Fonseca, J., Lima, E., Pallini, A. and Sabelis, M. (2008). Parasitoid Increases Survival of Its Pupae by Inducing Hosts to Fight Predators. PLoS ONE, 3(6), p.e2276.

This post was written by Niamh Dalton

Arthrophaga myriapodina

The forests around Ithaca, New York is the scene of an arthropod murder mystery. The killer seems to cover their track well and leave no obvious clues behind - aside from the dried, empty husk of dead millipedes clinging to the top of fence posts, branches, and fallen logs. So who or what is the macabre killer leaving the desiccated corpses of millipedes in prominent places? There are pathogens with similar modus operandi that infect and mummify insects; most of them are fungi, and a few of them have been previously featured on this blog, the most well-known example being the "zombie ant fungus". So what is the identity of this millipede killer?

(A) Typical posture of zombified millipedes infected with Arthrophaga myriapodina, (B, C) fungal structures erupting from between the segments of zombified millipedes. Photos from Fig. 3 of the paper

To find out, a group of scientists collected zombified millipedes and examined their fungal infection in detail using microscopes and by sequencing specific sections of their DNA which are used to identify and distinguish different fungi species. With this, they were able to identify and describe the zombie millipede fungus - they named it Arthrophaga myriapodina. This fungus that belongs to a group called the Entomophorales - a group of fungi consisting mostly of insect killers. For example a few months ago, I wrote about another entomophorale fungus that zombifies soldier beetles.

But A. myriapodina is the first species of that group documented to target millipedes. And while this study is the first time that this fungus has been formally described in detail and given a scientific name, such "zombie millipedes" have been known from as long ago as 1886, with some specimens stored in herbarium collections dating back from the early 20th century.

Given this millipede-infecting fungus has had such a long, but under-studied history, these scientists compared their freshly collected zombie millipedes with similar specimens held in museum collections, along with photographs of similar zombified millipedes hosted on sites such as Flickr, BugGuide, iNaturalist and other online photo-sharing sites. Through the combination of collecting fresh specimens, examining museum collections, and searching for online photos, they were able to establish that this fungus is found throughout Northeastern North America, with a few sighting from Texas and California.

As mentioned above, A. myriapodina has a modus operandi similar to many fungi that infect insects. The fungal spores find their way into the host's body and proliferate, eventually taking over the host entirely. When the fungus is ready to reproduce, it changes the host's behaviour so that it would carry it to a position that maximise spore dispersal. For A. myriapodina, this means anywhere elevated, whether it is the top of a fallen log, tree branches, or bridge abutments. Once in position, the fungus  emerge from the zombified millipedes in the form of powdery masses that seep out from between the segments. After they have dispersed their spores, the remaining fungal mass withers away, leaving an empty corpse and a fairy ring of infective spores.

The climbing behaviour that A. myriapodina induces in millipedes is comparable to those caused by zombie ant fungi. It is also a remarkable example of convergent evolution with a group of viruses known as baculoviruses which infect caterpillars and cause them to climb to their deaths. Those viruses induces a syndrome called Wipfelkrankheit or "treetop disease" that makes infected caterpillar climb to a high place before melting their bodies and raining droplets of virus-laden caterpillar goo into the forest canopy.

The emergence of zombie millipedes also seems to be weather dependent, because they are typically sighted a day or two after a bout of heavy rain. Perhaps heavy inundation acts as a trigger for the fungus to produce its spores. More research is needed to understand how rainfall and other seasonal pattern affects the life-cycle and outbreak of this fungal killer.

Reference:
Hodge, K. T., Hajek, A. E., & Gryganskyi, A. (2017). The first entomophthoralean killing millipedes, Arthrophaga myriapodina n. gen. n. sp., causes climbing before host death. Journal of Invertebrate Pathology 149: 135-140.

P.S. Some of you might know through my activities on Twitter (@The_Episiarch) that when I'm not writing these posts on new scientific papers about parasites, I also do illustrations, many of which are inspired by parasites and for the last two years I have been doing a series of illustrations known as "Parasite Monster Girls". So in keeping with the theme of this post, my most recent piece is Cordelia - a Parasite Monster Girl version of Cordyceps-infected zombie ants.

Eryniopsis lampyridarum

Mind-controlling fungi that manipulate ants have become quite well-know among the general public due to their ability to induce a "zombie-like" state in their host, but ants are not the only insects that can get infected by fungi, nor are they the only insects to get mind controlled by them. The study featured in this post is about a zombie beetle fungus call Eryniopsis lampyridarum which infects the goldenrod soldier beetle. Despite its name, the goldenrod soldier beetle is not as formidable as its name might indicate. The name is actually based on the first described soldier beetle species which has a colour pattern that resembles the coat of 17th-19th century British soldiers.

From Fig. 2 of the paper

The presence of E. lampyridarum in these beetles has been known for over a century, but relatively little research has been conducted on this pairing aside from some basic ecological research conducted in the 1970s and 1980s. It was not until now that someone has investigated this parasite-host interaction in close details, and provide descriptions of the fungal structure

From Fig. 4 & 5 of the paper

When the fungal infection in a beetle ripens, the infected insect will seek out a flower and clamp their mandibles around it in a vice-like grip. This is rather reminiscent of some zombie ant fungi which cause their hosts to position themselves on the underside of leaves where they can sprinkle spores into the path of uninfected ants. But the zombie beetles don't clamp themselves to leaves, nor do they bite down on just any old flowers, they only chose those from the Asteraceae - better known as daisies. After biting down on a daisy, the infected beetle succumbs to the infection. But the fungus is not done with its host quite yet.

Slowly, the dead beetle's wing covers and wings unfurl throughout the night, revealing a bloated abdomen brimming with fungal growth. By dawn the wings and their covers are full extended. So why have daisies as the final resting place for these zombie beetles? Also why unfold the wings and their covers at night just before daybreak?

For soldier beetles daisies, are like pubs or cafe - that's where they congregate to feed and possibly socialise with other beetles. So by placing itself on a flower, the zombie beetle is in prime position to meet its uninfected cousins. Unlike the zombie ant fungus which sprinkle its spores onto the ground to infect foraging worker ants, the spores of E. lampyridarum stays on the zombie beetle because that's where uninfected beetles are likely to come into contact with them.

With the fungal bodies sprouting from the abdomen, it seems that unfolding the wings would help expose the infective spores to potential host. However, there might be another reason for the wings to be unfolded. The researchers of this study suggested it actually serves the function of making the fungus-ridden corpse more attractive to uninfected beetles. Having the zombie beetle's wings open just before daybreak is also tailored to suit the daily routine of these beetles which are more likely to visit daisies in the morning. You can imagine that an unsuspecting goldenrod soldier beetle would visit a flower for a drink in the morning, meet some attractive looking beetles while it is there, only to end up with a fungal infection that will eventually take over them in body and mind

While some degree of mind-control is involved in getting the beetles to bite down on flowers, unfolding the wings seems to be a purely mechanical process. The wing unfolds long after the host has died, but the fungal growth propagate in such a way that it pushes the connective tissue at base of the beetle's wings and forces them to unfold. The fungus acts like the hand in a puppet, animating the beetle's dead body as if it is some kind of chitinous marionette.

But not all the infected beetles eventually become flower-clampers, some infected beetles simply die without ever climbing onto or clamping onto a daisy. In that case, the beetle are filled with thousands of resting spores, which unlike the ones on the zombie beetles, are not immediately infective. But those spores can last for a long time in the environment. For those beetles, when their bodies hit the ground and are broken apart by scavengers and microbes, they end up seeding the soil with a bank of viable spores.

So whereas the purpose of the infective spores on those flower-clamping zombie beetle is to spread the infection far and wide in the moment, those resting spores are an investment for the future - they are hardy and resistant, and their purpose is to wait in the soil for the next season, when they will unleash a brand new wave of zombifying plague.

Reference:
Steinkraus, D. C., Hajek, A. E., & Liebherr, J. K. (2017). Zombie soldier beetles: Epizootics in the goldenrod soldier beetle, Chauliognathus pensylvanicus (Coleoptera: Cantharidae) caused by Eryniopsis lampyridarum (Entomophthoromycotina: Entomophthoraceae). Journal of Invertebrate Pathology 148: 51–59

Ophiocordyceps pseudolloydii

The Cordyceps fungus has become a fixture in popular media, at least as the go-to comparison/cause for fictional human zombies. The nominal Cordyceps that most people think of is probably Ophiocordyceps unilateralis - the infamous "zombie ant fungus". But what most people don't realise is that there isn't just "the Cordyceps fungus" - that is just a single species out of many ant-infecting fungi in the Ophiocordyceps genus. That's right - there are multiple species of zombie ant fungi and they are all different. Each of them have evolved their own ways of getting the most out of their ant hosts.

Photo of infected ants from Fig. 1 and Fig. 2 of this paper

The species featured in today's blog post is Ophiocrodyceps pseudolloydii, and it is found in central Taiwan. This fungus specifically targets a tiny ant called Dolichoderus thoracicus. In the forest of central Taiwan are so-called "ant graveyards" - areas with high density of Cordyceps-infected zombie ants. Such sights are familiar to scientists who study these ant-fungi relationships, indeed, such "ant graveyards" have been found in other parts of the world where ants and Cordyceps fungi co-occur.

A group of scientists set out to document the behaviour and position of ants which have been mummified by O. pseudolloydii. One key thing they observed was that no matter where the zombie ants were found in the forest, the head of the dead ant tends to be pointed towards the direction of openings in the forest canopy. This indicates that the fungus might be using sunlight that comes through the canopy as a cue to steer the host ants into position.

Like other ant-infected Cordyceps fungi, O. pseudolloydii places the host ant in a position which is ideal for spreading its spores, without being dried out in open air. This usually means placing the ant underneath a leaf. But the fungus needs some way of anchoring the ant to the leaf before it can mummify the host and start sprouting into a fruiting body. Ophiocordyceps unilateralis induces a "death grip" in the zombified ants, whereby the ant locks its mandible around the vein of a leaf to secure it in place.

But O. pseudolloydii does not do that - instead of using the ant's mandible, O. pseudolloydii simply sprout a dense mass of fungal tissue which binds the ant to the underside of a leaf. So why doesn't it simply do what its more famous cousin does and make the ant bite down on a leaf vein? Possibly because the ant which O. pseudolloydii infects is much smaller than the carpenter ant which O. unilateralis parasitises. Compared with the carpenter ant workers which can grow up to 25 millimetres (about an inch) in length, the workers of D. thoracicus are merely 4 millimetres long. With such a tiny host a dense mat of fungal tissue is enough to anchor the ant in place.

By doing so, this might allow the fungus to save on making the mind-altering chemical to induce the leaf-vein biting behaviour, which can possibly allow it to produce more spores instead. All Ophiocordyceps pseudolloydii needs to do is make sure the ant is intoxicated enough to crawl to the right spot, and once that is done, the fungus will take care of the rest.

Reference:
Chung, T. Y., Sun, P. F., Kuo, J. I., Lee, Y. I., Lin, C. C., & Chou, J. Y. (2017). Zombie ant heads are oriented relative to solar cues. Fungal Ecology 25: 22-28.

Leucochloridium paradoxum (revisited)

Parasites manipulating their hosts' appearance and behaviour is one aspect of parasitology which seems to have captured the public's imagination. The idea of body-snatching parasitic horrors taking over a host in both body and mind is one that evokes (and exceeds) the scenarios of many horror movies. Among the more well-known example of such parasitic body-snatchers is Leucochloridium paradoxum - the infamous zombie snail parasite, also referred to as the "green brood sacs".

But while L. paradoxum is the most well-known among its kind, it is just one of about a dozen different species in the Leucochloridium genus, all of which infect small land snails (mostly amber snails) and produce the pulsating brood sacs that people recognise. Traditionally, scientists have used the different colours and shapes of the brood sacs to tell apart different Leucochloridium species. More recently, this has been supplemented with genetic analysis, which has confirmed the validity of using brood sac colour and shape for species identification.

Left: A snail infected with two different Leucochloridium Right: Broodsacs of L. paradoxum and L. perturbatum from a double-infected snail
Photos from Fig. 1 of this paper 

In this study, researchers from Russia apply both techniques to examine cases of multiple Leucochloridium infections. Yes, as if being host to a single species of mind-manipulating parasite isn't bad enough, an amber snail can get infected with two (or more)! The researchers examined snails collected from the town of Lyuban in Russia, and upon dissecting them, found that while most of the infected snails were parasitised by the infamous L. paradoxum, a few snails had both L. paradoxum (green brood sacs) and another species call L. perturbatum (brown brood sacs). While simultaneous infections of different flukes species in snails are not uncommon, they also came across the first recorded case of a snail that was infected with three Leucochloridium species - L. paradoxum, L perturbatum, and the third species L. vogtianum which aren't as colourful, but was covered in warty projections

In other trematodes, competition between fluke asexual stages within the snails usually end up with one species overwhelming the other and gaining monopoly on the host. So it is possible that those snails that harboured multiple infection were merely be in the middle of a transitional state before one of the parasite colony is eliminated by the other. Had the snail been examined much later on, it might have revealed only a single parasite colony without any traces of a prior cohabitation with another species.

What most people might not know about Leucochloridium is that the prominent brood sacs are merely a part of an asexually-produced parasite colony inside the host snail. Unlike the asexual stages of many other trematodes which exist as genetically-identical but physically discrete stages call sporocysts or rediae, the asexual stages of Leucochloridium are stitched together into a writhing mass. This living colony is differentiated into different parts in a way that is comparable to the colonies of siphonophores such as the Portuguese Man'O'War. At centre of the parasitic mass, deep inside the snail's body, is where embryonic parasites are produced. As the embryos develop, they move through the colony's branches and into the extremities that form the colourful brood sacs, each packed full of mature parasite larvae that are ready to infect a bird.

This study also revealed another observation which provides insight into how these parasites reach the bird final host. The usual story is that infected snail are manipulated by the parasite into crawling to an exposed location where they can be easily spotted by hungry birds. The bird then mistaken the snail's pulsating, brood sac-engorged eyestalks for caterpillars, and peck them off. This is a classic story of parasite manipulation, told many times in multiple books and documentaries. While the validity of this story was partly demonstrated in 2013 when a study was published showing snails infected with Leucochlordium are indeed attracted to exposed and well-lit locations, it has yet to be demonstrated whether this actually enhance the likelihood of them (or at least their parasite) being eaten by birds

Broodsacs of L. paradoxum leaving the host snail. From Fig. 1 of this paper

But the researchers in this study observed that those pulsating brood sacs are not limited to expressing themselves in the snail's eyestalks. These sacs of parasite larvae can in fact leave the snail - possibly by rupturing through the snail's body wall. If the brood sacs of these parasites can exit the snail on their own and remain viable while still pulsating in the outside world for a brief period of time, then that significantly alter the above oft-repeated narrative of how this parasite is transmitted to its final host.

The parasitised snails might not need to have its eyes pecked out by the bird for Leucochloridium to reach its final host after all. Instead of treating the snail as a sacrificial lamb, the parasite could be using it as a unwitting courier that brings itself to an exposed location, drop off a few brood sacs, then those twitching brood sacs would attract the attention of a hungry bird on their own. It is still not a pleasant life for the infected snail - it is still stuck with a constantly regenerating parasite colony which is taking up almost a quarter of its body mass, but at least Leucochloridium would not be adding further injuries to insult by soliciting a avian attack.

Reference:
Ataev, G. L., Zhukova, A. A., Tokmakova, А. S., & Prokhorova, Е. E. (2016). Multiple infection of amber Succinea putris snails with sporocysts of Leucochloridium spp.(Trematoda). Parasitology Research 115:3203–3208.

P.S. Leucochloridium is a very striking-looking parasite and has been subjected to numerous artistic interpretations, so here's one of my own in the form of a Parasite Monster Girl version of a Leucochloridium-infected snail.

Tylodelphys sp.

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

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

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

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

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

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

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

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

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

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

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

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

Anomotaenia brevis

There are many examples of parasites altering the behaviour of their hosts, and some of them turn their hosts into functionally different animals compared with their uninfected counterparts. When this occurs in highly social animals, this effects can cascade onto other members of the group. Anomotaenia brevis is a tapeworm which happens to be one of many parasite species which have been documented to modify their host's appearance and/or behaviour in some way.

Photo by Sara Beros, used with permission

While the adult tapeworm lives a pretty ordinary life in the gut of a woodpecker, the larva uses a worker ant as a place to grow and a vehicle to reach the bird host. Specifically, they infect Temnothorax nylanderi - a species of ant found in oak forests of western Europe. These ants nest in naturally occurring cavities in trees such as sticks or acorns and the colony consists of a single ant queen surrounded by several dozen worker ants. These ants are a regular part of the woodpecker's diet so there's a fairly reasonable chance that the tapeworm will reach its final destination if it waited around for long enough. But A. brevis is not content with just leaving it to chance.

Worker ants can become infected through eating bird faeces which are contaminated with the parasite's eggs. As the tapeworm larvae grow inside the ant's body, these infected worker ants become noticeably different from their uninfected counterpart; they smell different (determined by the layer of hydrocarbon chemicals on their cuticle), they're smaller, they have yellow (instead of brown) cuticles, spend most of their time sitting around in the nest, and for some reason their uninfected nestmates are more willing to dote on these tapeworm-infected ants rather than healthy ones. They essentially become a different animal to the healthy workers, and other ant parasites have been known to alter their host to such a degree that parasitised individuals were initially mistaken as belonging to an entirely different species.

When scientists investigated the prevalence of A. brevis in nature, they found that about thirty percent of the ant colonies they came across have at least some infected workers. While in some nests only a few of the workers are infected, in other cases over half the workers are carrying tapeworms. Furthermore, they also found a few of the workers (2%) were infected but had yet to manifest the symptoms associated A. brevis. When over half the work force of a colony is under the spell of a body-snatching parasite, that must affect the colony in some way. So how does this affect the ant colony as a whole?

During their development, infected ants have higher survival rate and far more of them (97.2%) reach adulthood compared with uninfected (56.3-69.5%) ants. This make sense from the perspective of the parasite's transmission as it needs its host to stay alive for as long as possible to get inside a woodpecker. But it seems to also affected their uninfected sisters because uninfected worker ants in a colony which has parasitised workers also have lower survival rates than those from colonies free of any tapeworm-infected ants. But A. brevis also affects the colony's functioning in other ways as well.

The scientists behind the paper being featured today conducted a series of experiments where they manipulated the composition (and in doing so, parasite prevalence) of experimental ant colonies. Since T. nylanderi colonies regularly experience take-over and/or merging with other colonies, introducing or remove new ants into the experimental colonies would not cause them to exhibit unnatural behaviours as it is not too different what would usually occur in nature anyway. They set up colonies with different proportion of A. brevis-infected workers and tested how they responded to different types of disturbances.

They simulated a woodpecker attack by cracking open the experimental ant nests and seeing how long it took for them to evacuate. Under a simulated attack, about half of the healthy worker escaped (48-58.9%) but very few of the tapeworm-infected workers escaped (3.2%), which is exactly what the tapeworm wants - remember, the parasite needs to be eaten by a woodpecker to complete its lifecycle - so when one comes knocking, the tapeworm gets it host to sit tight and prepared to be sacrificed.

They also simulated intrusion from ants of a different colony or species by pitting individual invading ants against their experimental colonies. These invaders consisted of a mix of infected and uninfected individuals from nests which contained some or no infected nestmates. When confronting ants from other colonies, they were the most aggressive against the intruder if it was of a different species (in this case, T. affinis), but when it comes to other T. nylanderi ants, they responded more aggressively if the intruder from a different colony was harbouring tapeworm larvae.

In contrast, they were pretty chill about the presence of tapeworm-infected ants if it was one of their own nestmate. But the tapeworm also affected colony aggression in another way - the research team noted that colonies with many infected workers were also less aggressive overall towards any invaders. Not only does A. brevis alter its host's appearance and behaviour, it also seem to cause the host's nestmates to be more chilled out.

Parasites can manipulate their host in some astonishing ways, and the host's altered behaviour and/or appearance has been described as the parasite's "extended phenotype". But when the host is a social animal that is surrounded by many other group members, the parasite's influences can extend well beyond the body of its immediate host, and manifest in the surrounding kins and cohorts as well.

Reference:
Beros, S., Jongepier, E., Hagemeier, F., & Foitzik, S. (2015). The parasite's long arm: a tapeworm parasite induces behavioural changes in uninfected group members of its social host. Proceedings of the Royal Society B 282: 20151473

Chordodes formosanus

For most insects (and other small animals), the praying mantis is a creature out of their worst nightmare; a deadly predator with giant compound eyes, a nasty set of high-speed spiky grasping limbs, and an appetite to boot. But Chordodes formosanus is a parasite that would give mantis nightmares - it is a hairworm - and regular readers of this blog will know immediately why that is justified.

From Fig. 2 of this paper

The worm starts out as a microscopic larva hidden inside the body of small insects - the mantis' usual prey - but once it is ingested by a mantis, it can then grow to several centimetres long inside its abdomen. By the time it is ready to bid farewell to its reluctant host, which comes when it reaches sexual maturity, the worm has already taken up most of the space within the mantis, leaving it a half-empty husk. The modus operandi of a horsehair worm is to then get into the water, which involves the host taking a dunk - whether it wants to or not. Apart from commandeering the mantis to go for a terminal end to their relationship, during the worm's development, it takes a massive toll. After all, one does not simply host a giant worm inside one's abdomen without any consequences.

But the said consequences is not equally distributed within the mantis population - this hairworm seems to affect male mantis more severely - especially in regards to their reproductive capacity. In a nutshell - C. formosanus shrink their testes and in some cases, they disappear altogether. However, this parasite seems more forgiving when it comes to female mantis; infected female mantis can harbour the worm and still retain intact reproductive organs. Not to say it doesn't exact a toll, just that the female mantis can still have some babies before her end comes. So why this sex bias? The reason lies in how this parasite alters the host's physiology.

When researchers looked at various aspects of the infected mantis' physical appearance, they also noticed some external changes in both sexes - they had comparatively shorter walking legs, smaller wings, and altered antennae - but it was more pronounced in the infected male mantis. Overall, the infected individuals have an appearance which bears closer resemblance to that of late-stage juvenile rather than adults. This suggest that C. formosanus might be tempering with the mantis' so-called "juvenile hormones" which control development in insects. But why is it that only the male mantis lose their reproductive organs? At this point, it is not entirely clear, but it might have something to do with the different role played said hormones in the development of each sex.

So why has C. formosanus evolved to castrate their male mantis host? From the parasite's perspective, host castration is a very effective strategy - the host does not need its gonad to survive, only to reproduce. So by tapping into this energy source, the parasite can keep the host alive while maximising the amount of resources it draws from the host.

For that, the host pays a double cost in terms of evolutionary fitness. Usually with such parasite infection which inevitably results in the host's death, the best thing for the host to do to make the best of a bad situation and reproduce as much as possible before they are eventually killed by the parasite. But in this case, the male mantis doesn't even get to do that - thanks to C. formosanus, long before it bid farewell to life, it has to bid farewell to its junk as well

Reference:
Chiu, M. C., Huang, C. G., Wu, W. J., & Shiao, S. F. (2015). Morphological allometry and intersexuality in horsehair-worm-infected mantids, Hierodula formosana (Mantodea: Mantidae). Parasitology 142: 1130-1142

Polysphincta boops

This is the sixth post in a series of blog posts written by students from my third year Evolutionary Parasitology unit (ZOOL329/529) class of 2015. This particular post was written by Rebecca-Lee Puglisi about not one, but THREE spider-zombifying and how they differ in their host preference, as well as what kind of web they make their spider hosts weave (you can read the previous post on how parasites mess with the Monarch Butterfly's migration here).

Photo of Polysphincta boops by Hectonichus

We all know that the natural world is amazing, and we all know that I hate horror movies! But what if losing ones self control and being manipulated by another was actually happening today and not just something you saw in movies? Let’s set the scene here. You are minding your own business when a six legged monster jumps upon your back, stabbing and poisoning you, knocking you unconscious for a few moments. When you wake up, you're no longer yourself and under control by the monster until the day you die. This nightmare happens on a daily basis to Orb-Weaver Spiders (Araneus and Araniella) in nature thanks to parasitoid wasps (Polysphincta and Sinarachna) that use them as hosts.

A study published last year in the journal Ecological Entomology aimed to identify whether the variations in host response to manipulation is a result of differences among parasitoids or among the spiders themselves. Spiders and wasps were collected at four different locations over Europe by shaking trees and catching the spiders and wasps in large nets underneath. The researchers collected four species of spiders (Araneus diadematus, Araniella cucurbitina, Araniella displicata, and Araniella ophistographa), and three species of parasitoid wasps (Polysphincta boops, Polysphincta tuberose, and Sinarachna pallipes), and 417 spiders were collected in total and placed into a laboratory in separate arenas where different species of wasps were introduced.

They found that while Polysphincta boops only parasitised one spider species - A. ophistographa, its relative P. tuberose was less picky and parasitised three spider species - A. cucurbitina, A. opisthographa, and A. diadematus. The same goes for S. pallipes, which parasitised A. cucurbitina, A. displicata, and A. opisthographa. All these wasps sting the spiders, paralysing them to lay an egg on their abdomen. The spider awakes with the egg that then hatches and feeds on the spiders' hemolymph (its blood), and the spider continues its life as normal.

Left: Web woven by spider parasitised by Polysphincta. Right: Web woven by spider parasitised by Sinarachna
Photos from Fig. 2 of the paper 

Their experiments showed that the parasitised spider’s webs changed from a two-dimensional to a three-dimensional structure with difference in the densities of the webs and the cocoons created. The differences between the webs / cocoons are determined by the final instar larva of the wasp species when neuromodulator chemicals are injected in the host spider by the larva. The spiders parasitised by Polysphincta wasps created a high density silk web with a low density cocoon web, whereas spiders parasitised by the Sinarachna wasps created the opposite structures, with a low density silk web and a high density cocoon web.

Higher density webs and cocoons provided better protection for the developing larva. After manipulating the spider to make the web and cocoon for the wasp larva, the larva then develops into its final stage where it kills the spider host, and eats all its internal organs before retreating into the web cocoon where it will grow into adult wasp. After the it reaches maturity, it will then find a mate to start the whole cycle again. This whole process takes roughly 20-30 days.

This whole circle of life and host manipulation interactions is both amazing and horrifying! I mean, have you seen the ‘chest buster’ scene from the movie ‘Alien’? If movie writers decide to make another big blockbuster about parasitoid creatures like those wasps, but have them attack humans, I will never sleep again!

Reference:
Korenko, S., Isaia, M., Satrapova, J., & Pekar, S. (2014). Parasitoid genus‐specific manipulation of orb‐web host spiders (Araneae, Araneidae). Ecological Entomology 39, 30-38.

This post was written by Rebecca-Lee Puglisi