Category: manipulation

Horsehair worm manipulates mantis with its own genes

Horsehair worms, which live parasitically in various insects during their larval stage, drive their host to suicide. Tappei Mishina and colleagues wondered how they acquired the potential to make this happen.

A striking and gruesome example of parasites that manipulate their host are horsehair worms. During their larval stage, they live in crickets, grasshoppers, and mantises, but as adult worms they live freely in water. To get there, they drive their hapless host to commit a self-destructive act: it jumps into the water. Horsehair worms can disrupt the behaviour of their host so dramatically thanks to genes they picked up from it, Tappei Mishina and colleagues show.

In water, adult horsehair worms (Nematomorpha) mate in a knotted mass of males and females; that is why they are also called Gordian worms. The females then lay eggs from which microscopic larvae hatch. In order to develop further, they must move to insect hosts that live on dry land. The hosts can ingest the larvae directly with their food or via a ‘transporter’, for instance a mayfly. Living in water during its larval stage, this insect is exposed to horsehair worm larvae. The adult mayfly flies out and may be grabbed by an insect host, which then becomes infected with a parasitic horsehair worm larva.

Horror

And then, a horror story starts. The horsehair worm larva grows into an extremely thin worm that can reach several times the length of the host. By the time the parasite matures, it forces its host to behave unnaturally. The host, no longer in charge of himself, starts wandering until it comes across water. Then it enters the water body, often with death as a result. If it survives, it will be infertile.

But the worm is in its element. It wriggles out of the insect’s body and starts looking for conspecifics. If the host is attacked by a predatory water insect before the worm is out, it will emerge more quickly. And if the host is swallowed by a fish or frog, the worm manages to escape from that fish or frog also.

How can horsehair worms so dramatically manipulate the behaviour of their hosts, from which they differ greatly from an evolutionary perspective, Mishina wondered.

His research on mantis Tenodera angustipennis and horsehair worm Chordodes fukuii shows that the worm literally took over the biochemistry of its host.

Expression pattern

The researchers first examined which genes are activated or deactivated in the horsehair worm and in the mantis brain, and how this pattern changes during host manipulation. They show that only in the worm does the expression pattern change: during manipulation, many genes are read and transcribed to be translated into proteins that were previously inactive, while other genes are silenced. The worm produces proteins to influence the praying mantis’ brain, is the conclusion.

They then compared genes from Chordodes species with information about known genes and proteins stored in databases. This yielded a surprising result: more than 1,400 genes of the parasites are very similar to genes of mantises. Especially these genes are expressed differently during manipulation; most are more strongly activated, others are suppressed. Other horsehair worm species than Chordodes species, which have other hosts, do not possess these mantis genes.

Horizontal gene transfer

It seems that Chordodes has picked up genes from its hosts, mantises, over the course of its evolutionary history – and not just a little. That happened not once, but many times. It is not surprising that the proteins encoded by these genes have an effect in mantises.

Gene transfer between animal species, which is called horizontal gene transfer, is a special and, as far as we know, very rare phenomenon. The researchers suggest that it may also play a role in other cases of host manipulation.

Willy van Strien

Photos: ©Takuya Sato
Large: mantid Tenodera angustipennis
Small: mantid Tenodera angustipennis and Chordodes horsehair worm

A horror video with horsehair worms on YouTube

Sources:
Mishina, T., M-C. Chiu, Y. Hashiguchi, S. Oishi, A. Sasaki, R. Okada, H. Uchiyama, T. Sasaki, M. Sakura, H. Takeshima & T. Sato, 2023. Massive horizontal gene transfer and the evolution of nematomorph-driven behavioral manipulation of mantids. Current Biology, online 19 October. Doi: 10.1016/j.cub.2023.09.052
Sánchez, M.I., F. Ponton, D. Missé, D.P. Hughes & F. Thomas, 2008. Hairworm response to notonectid attacks. Animal Behaviour 75: 823-826. Doi: 10.1016/j.anbehav.2007.07.002
Ponton, F., C. Lebarbenchon, T. Lefèvre, D.G. Biron, D. Duneau, D.P. Hughes & F. Thomas, 2006. Parasite survives predation on its host. Nature 440: 756. Doi: 10.1038/440776a
Biron, D.G., L. Marché, F. Ponton, H.D. Loxdale, N. Galéotti, L. Renault, C. Joly & F. Thomas, 2005. Behavioural manipulation in a grasshopper harbouring hairworm: a proteomics approach. Proceedings of the Royal Society B 272: 2117-2126. Doi: 10.1098/rspb.2005.3213

Lancet liver fluke turns ant into zombie, but not during the day

Larvae of the lancet liver fluke, a parasite, have to transfer from ant to deer. They manipulate the behaviour of infected ants to maximize the chance of transmission, Simone Nordstrand Gasque and Brian Fredensborg report.

An ant carrying lancet liver fluke larvae is no longer itself. At the parasite’s command, it climbs up in the grass and stays there motionless. This makes it more probable for the parasite to reach the host in which it matures, a grazer. The manipulation is complex, as Simone Nordstrand Gasque and Brian Fredensborg show: an infected ant only remains high up in the vegetation when it is chilly; when it is warm, it comes back and behaves normally.

The lancet liver fluke (Dicrocoelium dendriticum, a flatworm) has a complicated life cycle with three larval stages in three different hosts; it cannot live outside a host. It develops successively in a land snail, an ant, and a grazing mammal, such as a deer, sheep, or a cow. So, it has to transfer several times.

Bile ducts

Adult liver flukes live in bile ducts in the livers of grazers. They mate and produce eggs that are excreted with the feces. The eggs are picked up by a land snail that nibbles on the droppings. The eggs hatch in the snail’s body into so-called miracidium larvae. They multiply asexually and thousands of larvae of the next stage, the cercaria larvae, appear. They migrate to the snail’s lung where they are packed in slime balls.

The snail coughs up the slime balls, and then it is the turn of the next host, which also comes by itself: the slime balls are tasty snacks for ants, which take them with them to their nest. Adult ants and larvae consume the balls and become infected. In ants, the cercaria larvae develop into the next stage, the metacercaria larvae.

Sacrifice

Now comes the most difficult transmission, which is necessary to complete the cycle: from ant back to grazer. That doesn’t happen easily. Ants reside in their nest or walk around on the ground. A grazer does not take a bite of that. The cycle could stop here, but now the parasite intervenes.

The larvae – there may be hundreds of them –safely encapsulate in the ant’s abdomen. But one of them moves to a ganglion in the ant’s head. It is unclear exactly how it manages, but this larva gains control over the ant’s behaviour. Like a zombie, the ant climbs up a blade of grass for no reason and locks its jaws to the vegetation. And so, a grazer may ingest the ant with the larvae on board along with the grass.

The larva that enabled the transfer dies in the grazer’s stomach. It sacrificed itself for the others, which emerge from their capsule in a safe place, develop into adult worms and settle in the bile ducts of the grazer: the circle is complete.

It is extraordinary that a parasite changes the behaviour of its host so drastically. But the lancet liver fluke does even more: it makes sure that the change is only expressed when it makes sense.

Sophisticated

Gasque and Fredensborg conducted research into the behaviour of the European red wood ant (Formica polyctena) after infection with lancet liver fluke in woods in Denmark, where roe deer live. They show that an infected ant only stays high up in the vegetation when it is cool, i.e., early in the morning and in the evening. During the day, it unlocks its jaws, goes down and behaves like the other ants.

It turns out that the temperature determines whether an infected ant is itself or becomes a zombie. Time of day, humidity and amount of sunlight do not matter. The warmer it is, the fewer infected ants persist in their biting behaviour. Only on chilly days at the end of the season, do many infected ants stay attached to vegetation all day.

This is beneficial from the parasite’s point of view. Because on hot days an exposed ant could overheat and die, and then the parasitic larvae would not survive either. Since deer mainly graze at dusk, there is no point in taking that risk. It is better to release the ant and let it ant behave normally, and only send it back up again in the evening.

Willy van Strien

Photos:
Large: infected European red wood ant, Formica polyctena. ©Simone Nordstrand Gasque
Smal: lancet liver fluke (Dicrocoelium dendriticum), adult. D. Drew (Wikimedia Commons, Public Domain)

Source:
Gasque, S.N. & B.L. Fredensborg, 2023. Expression of trematode-induced zombie-ant behavior is strongly associated with temperature. Behavioral Ecology, online 24 August. Doi: 10.1093/beheco/arad064

Dead host helps parasitoid wasp escape from crypt

The parasitoid wasp Euderus set lays its eggs near oak gall wasps that develop within their gall. The parasitoid larva will consume its host. But first, the larva manipulates it into performing a nasty task. Otherwise the parasitoid would be buried alive in the oak gall.

The North American parasitoid Euderus set is a natural enemy of gall wasps that develop within galls on oak trees.  It does not attack all oak gall wasps species; hundreds of oak gall wasp species live in North America. But at least seven species fall victim, as Anna Ward and colleagues report.

The researchers discovered the wasp several years ago and named this ‘crypt-keeper wasp’ after Seth, the Egyptian god of darkness and chaos. According to some sources, Seth killed his brother Osiris by trapping him in a tailor-made sarcophagus and throwing him into the Nile. The behaviour of the parasitoid  wasp is as naughty. One of the victims is the oak gall wasp Bassettia pallida, and the researchers described what happens to the galler when Euderus set appears on the scene.

Head stuck

The gall wasp female lays her eggs under the bark of young oak branches. A branch then is induced by the gall wasp to form a separate crypt for each egg, in which the wasp will develop into a larva, pupa and adult. A gall develops in the branch. The adult gall wasp has to chew its way out through woody tissue and bark.

The researchers found holes in oak branches through which an adult gall wasp had emerged. But they also discovered holes in which the head of a gall wasp was stuck. It was a mystery: why did the gall wasp sometimes get stuck?

On inspection, they found a stranger in the chamber behind stuck gall wasp heads: a larva or pupa of a parasitoid, which had consumed the gall wasp partially or completely. That parasitoid was Euderus set. In some cases, the stuck gall wasp head was pierced; the chamber behind such head was empty, except for the remains of the gall wasp.

Nasty task

Here is what happens, according to the authors: a female parasitoid lays an egg in the chamber of a developing gall wasp; after hatching, the parasitoid larva will eat its gall wasp host when it has reached adult stage. But first, it makes the host do some work. The parasitoid induces the young gall wasp to excavate an emergence hole that is narrower than normal. As a result, the gall wasp gets stuck as soon as its head reaches the surface; the head plugs the exit hole. The parasitoid then consumes its host entirely, pupates, emerges as adult parasitoid and leaves the chamber via the empty body and stuck head of the gall wasp.

Rescue

How the parasitic wasp manipulates the behaviour of its host, is still unknown. But it is to its advantage, because there is little chance that it can chew its own way out through woody plant tissue and bark, as experiments showed. Without a passage in the form of the empty gall-wasp body and head, the parasitoid wasp would be buried alive.

Now, Ward showed that not only Bassettia pallida, but at least six other oak gall wasp species can be attacked by Euderus set. They live in similar galls that are integrated with an oak branch or leaf and that have no structures to keep enemies out, such as spines. This makes makes them vulnerable to Seth.

Willy van Strien

Photo: Andrew Forbes

On YouTube, the research group explains how parasitoid Euderus set manipulates its host

Sources:
Ward, A.K.G., O.S. Khodor, S.P. Egan, K.L. Weinersmith & A.A. Forbes, 2019. A keeper of many crypts: a behaviour-manipulating parasite attacks a taxonomically diverse array of oak gall wasp species. Biology Letters 15: 20190428. Doi: 10.1098/rsbl.2019.0428
Weinersmith, K.L., S.M. Liu, A.A. Forbes & S.P. Egan, 2017. Tales from the crypt: a parasitoid manipulates the behaviour of its parasite host. Proc. R. Soc. B 284: 20162365. Doi: 10.1098/rspb.2016.2365

How parasitic thorny-headed worm reaches the right host

When fresh water shrimp is parasitized by thorny-headed worm, the parasite is visible from the outside as an orange dot. Thanks to this striking spot, fish will easily detect the shrimp and ingest it, whereupon the parasite completes its development in the fish. According to Timo Thünken and colleagues, only fish that are suitable as hosts preferentially swallow infected shrimp.

The thorny-headed worm Pomphorhynchus laevis is a parasite with a complex life cycle, which takes place in fresh water. During the first part of that cycle, it develops within fresh water shrimp Gammarus pulex, after the shrimp ingested parasite eggs from the water. The parasite develops to a certain stage, the cystacanth.

When the parasite has reached that stage, Gammarus no longer can serve as a host. The parasite has to switch to fish to be able to complete its life cycle. In the new host, the parasite hooks onto the intestinal wall, matures and reproduces. Female parasites produce eggs that are released together with fish faeces, completing the cycle.

The switch from shrimp to fish can happen in only one way: fish must ingest parasitized shrimp. Timo Thünken and colleagues show how the parasite manages this process.

Manipulation by thorny-headed worm

Normally, Gammarus pulex, no more than 2 centimetres in length, try to avoid being swallowed by fish. The shrimp hide in darkness, avoid areas with fish odour and have an inconspicuous colour.

But a parasitic thorny-headed worm that reached the cystacanth stage will intervene. It changes the behaviour of the host that it no longer needs; the shrimp leave darkness and show a preference for water with fish odour. Moreover, the mature cystacanth turns orange, being visible from the outside as an orange dot on the host.

Parasitized Gammarus seem to offer themselves as prey to fish: fish will easily encounter them and detect them. And indeed, they consume many parasitized shrimp, as was shown earlier in three-spined stickleback. For Gammarus, this is the end of the story, but for the parasite the future is opened.

At least …. if it has ended up in a suitable host. Not all fish species that prey upon Gammarus are a suitable host for the parasite. It will not survive in fish that exhibit an effective immune response. Manipulating Gammarus confers a lower net benefit if it also increases the chance of the parasite to end up in the wrong host.

Barbel suitable, brown trout not

Now, Thünken shows that the manipulation is effective: only suitable host fish ingest a relatively large amount of parasitized Gammarus.

He discovered this in experiments in which he painted an orange dot on unparasitized shrimp, so that they looked like shrimp carrying a ripe cystacanth. He then offered these shrimp, together with unpainted conspecifics, to a number of fish species. The painted shrimp were not really parasitized, and so they behaved the same as the unpainted ones. In this way, Thünken was able to check whether all fish species, just like stickleback in the earlier experiments, preferentially eat coloured prey.

In another experiment, he fed parasitized Gammarus to fish. Four months later, he checked if the fish were carrying living parasites, in order to assess which fish species are suitable hosts.

One of the fish species used, barbel, mainly consumes Gammarus with an orange dot, as it turned out, so this fish will easily get infected with the parasitic thorny-headed worm. This is beneficial for the parasite, because barbel turned out to be a very suitable host.

Brown trout, on the other hand, was as likely to swallow painted Gammarus as unpainted shrimp; the colour change had no effect on this fish. That’s also beneficial, because brown trout turned out not to be a host in which the parasite can survive. The same findings – indifferent to the colour change, poor host – applied to two other fish species, perch and ruffe.

Beneficial

Conclusion: an orange dot on Gammarus has an effect on fish that can serve as host of the horny-headed worm, barbel as well as stickleback in the earlier tests. These fish consumed colour Gammarus relatively often. But for unsuitable fish – brown trout, perch and ruffe – it makes no difference whether their prey has an orange spot or not. So, the dot increases the chance that the parasite will switch to a suitable host without increasing the risk that it will end up in the wrong fish.

How the link between the fish’s sensibility to the prey colour and its suitability to act as host might have arisen, is another question which has not yet been answered.

Stickleback

Stickleback are suitable hosts, but they do not fully meet the pattern. In the new experiments, not all stickleback seem to preferentially consume Gammarus with an orange dot; some even avoided them. With regards to this fish species, the colour alteration of Gammarus can be counterproductive.

According to the researchers, this is because this small fish suffers more from parasitic infection than the other species, which are considerably larger. Stickleback living in an environment in which thorny-headed worm is abundant are likely to avoid infection by skipping coloured Gammarus prey from their diet, warned by the orange colour. For larger fish species, on the other hand, avoiding parasitic infection is not important enough to let prey go.

Willy van Strien

Photo’s: © Nicole Bersau/Uni Bonn
Large: fresh water shrimp Gammarus pulex with thorny-headed worm Pomphorhynchus laevis visible as orange dot
Small: adult thorny-headed worm

Sources:
Thünken, T.,  S.A. Baldauf , N. Bersau , J.G. Frommen & T.C.M. Bakker, 2019. Parasite-induced colour alteration of intermediate hosts increases ingestion by suitable final host species. Behaviour, online July 19. Doi: 10.1163/1568539X-00003568
Kaldonski, N., M.J. Perrot-Minnot, R. Dodet, G. Martinaud & F. Cézilly, 2009. Carotenoid-based colour of acanthocephalan cystacanths plays no role in host manipulation. Proceedings of the Royal Society B: 276: 169-176. Doi: 10.1098/rspb.2008.0798
Baldauf, S.A., T. Thünken, J.G. Frommen, T.C.M. Bakker, O. Heupel & H. Kullmann, 2007. Infection with an acanthocephalan manipulates an amphipod’s reaction to a fish predator’s odours. International Journal for Parasitology 37: 61-65. Doi: 10.1016/j.ijpara.2006.09.003
Bakker, T.C.M., D. Mazzi & S. Zala, 1997. Parasite-induced changes in behavior and color make Gammarus pulex more prone to fish predation. Ecology 78: 1098-1104. Doi: 10.1890/0012-9658(1997)078[1098:PICIBA]2.0.CO;2

Twisted-wing parasites change the behaviour of host wasps

The life cycle of the parasite Xenos vesparum is closely linked to that of the wasps in which it lives. It modifies their behaviour in such a way that it meets its needs, as Laura Beani and colleagues demonstrate.

It is often creepy as well as fascinating to see how parasites control their host. A nice example is Xenos vesparum, parasite of the European paper wasp (Polistes dominula). Its manipulation skills are being unravelled by Laura Beani and her colleagues.

The parasite, which belongs to the insect group of twisted-wing parasites, has a bizarre life cycle, with a striking difference between males and females. In the larval stage, the parasite lives within a wasp host. Males pupate in their host; the front part of the pupae extrudes trough the cuticle between the plates of the host’s abdomen. When adult males emerge, they leave their host to live freely; within a day, they die.

Females live much longer. They remain in their host and don’t pupate, but turn into a ‘bag’ filled with egg cells and a fat supply. Only their cephalothorax, into which head and thorax are fused together, is tough and visible between the plates of the host’s abdomen. Usually only one parasite, either male or female, will mature in a parasitized wasp.

Male and female parasite must mate on the wasp in which the female lives. They do it fast.

Wasp colony

Xenos parasites effectively exploit the annual cycle of their host. In March, fertilized wasp queens, which have spent the winter in groups, awaken. Every queen occupies a place to establish a colony. She builds an open nest and lays the first eggs, which will produce workers. Before these eggs have developed into adults, the queen also has to collect food and take care of the brood. But later, from May, she is just laying eggs, while the workers, who don’t reproduce themselves, do the rest of the work.

In summer, the colony is flourishing with a maximum of fifty wasps, and it is time for the next step. The queen now starts laying eggs that will develop into males and sexual females, future queens. Males and sexual females (gynes) appear in July-August.

Overwintering

Then the queen has finished her task. She stops and the colony collapses. The gynes leave the nest and in early autumn, they aggregate in groups that attract males. Mating follows. As winter approaches, the fertilized gynes search for a sheltered place, again aggregating; they often cluster in buildings, for example under roof tiles. There they hibernate and wait for the spring. Males and worker wasps die before winter. In March, the new queens awaken from winter diapause and the cycle starts again.

The European paper wasp is a common species, and it is not as annoying as the common wasp, Vespula vulgaris.

Trumpet creeper

The parasite disturbs the role pattern of its host. But not immediately. In May, tiny parasite larvae penetrate into worker wasp larvae, which appear to be little affected by the presence of the parasite. Only when the hosts have developed into a pupa, the parasite larvae undergo a growth spurt and mature.

And then the manipulation starts: parasitized workers do not stick to their role. They are lazy and at the age of one week, they will leave the nest.

Beani, doing research in Tuscany, describes how in early summer the parasitized worker wasps are mainly to be found on trumpet creeper bushes; the trumpet creeper, originating from North America, has naturalized in Europe. It produces a lot of nectar, which the parasitized wasps enjoy. Healthy, non-parasitized wasps spend much less time on this plant. Because the hosts deserted the nest and moved to trumpet creeper, the parasites easily find a partner with which they can mate. In the wasp nest, mating would be impossible, as parasite males would immediately be chased off by healthy workers.

Castration by Xenos

Parasite embryos develop within the fertilized parasite females in a wasp’s body and new parasite larvae emerge at the end of July. A female parasite releases more than three thousand larvae which all need a host to develop. When healthy foraging wasps pass by, larvae cling to them, are transported to the wasps’ nest and start searching for wasp larvae. Among infected wasp larvae, there will now be putative males and sexual females, which were destined to reproduce. But they will never do the job, as the parasite castrates them.

Safe

From mid-July on, parasitized wasps (workers, males and gynes) form groups outside the nests, just like healthy young sexual females will do later in the season: the role pattern is erased. They gather on high plants and later on buildings, usually places where healthy males gather every year or where future queens use to overwinter. The parasitized wasps are inactive, the parasites have much opportunity to mate.

When healthy sexual wasp females fly out and aggregate, they often join these groups of parasitized wasps.

At the end of the season, when the gynes have been fertilized and gather at places to hibernate, wasps that contain a fertilized parasite female will join them. Parasite females safely spend the winter in a wasp body, in a group of wasps on a sheltered place. Wasps that carried a parasite male have no function anymore; they die in autumn.

Delivery

When healthy young queens leave to establish a colony in spring, parasitized wasps are left behind. A few weeks later, when the first wasp larvae have hatched in wasp nests, the parasites release their larvae. They then apply a last manipulative trick: they induce their host wasp to deliver the mature larvae in several young wasp nests. There are still no adult workers to defend these nests and the queen is often gone to collect food. From within her host, the parasite female drops larvae in the nests. She also drops some larvae on plants, as a foraging wasp may come along and take them with it.

And so the Xenos parasite completes the circle – with enforced cooperation of the host.

Willy van Strien

Photo: European paper wasp. ©Hans Hillewaert (Wikimedia Commons, Creative Commons BY-SA 4.0)

Xenos peckii mating on YouTube

Sources:
Beani, L., F. Cappa, F. Manfredini & M. Zaccaroni, 2018. Preference of Polistes dominula wasps for trumpet creepers when infected by Xenos vesparum: A novel example of co-evolved traits between host and parasite. PLoS ONE 13:e0205201. Doi: 10.1371/journal.pone.0205201
Beani, L., R. Dallai, D. Mercati, F. Cappa, F. Giusti & F. Manfredini, 2011. When a parasite breaks all the rules of a colony: morphology and fate of wasps infected by a strepsipteran endoparasite. Animal Behaviour 82: 1305e1312. Doi: 10.1016/j.anbehav.2011.09.012
Beani, L., 2006. Crazy wasps: when parasites manipulate the Polistes phenotype. Annales Zoologici Fennici 43: 564-574.
Hughes, D.P., J. Kathirithamby, S. Turillazzi & L. Beani, 2004. Social wasps desert the colony and aggregate outside if parasitized: parasite manipulation? Behavioral Ecology 15: 1037-1043. Doi: 10.1093/beheco/arh111