From so simple a beginning

Evolution and Biodiversity

Category: parasitism (Page 1 of 2)

Suicide on command

26 October 2023 /

Horsehair worm manipulates mantis with its own genes

Mantis Tenodera angustipennis is host of horsehair worms

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.

Chordodes horsehair worm is longer than its host

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

Only when the weather is cool

2 October 2023 /

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

lancet liver fluke manipulates ant into clamping onto a blade of grass

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 lancet liver fluke lives in bile ducts of grazers

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

Egg signature

21 August 2023 /

African cuckoo stands little chance with fork-tailed drongo

African cuckoo is not successful with fork-tailed drongo

African cuckoo females lay their eggs in nests of fork-tailed drongos. They mimic drongo eggs very accurately – and yet drongos recognize more than 90 percent of cuckoo eggs, Jess Lund and colleagues show.

South of the Sahara lives the African cuckoo, Cuculus gularis, which, like the common European cuckoo, lays eggs in the nests of other bird species (one egg per nest) with the intention that foster parents will raise their chicks. The brood parasite targets only a few bird species, of which the fork-tailed drongo, Dicrurus adsimilis, is one of the most important.

But the cuckoo has hardly any success with this important host species, Jess Lund and colleagues show. The intended foster mother usually notices the deception because she has put a ‘signature’ on her own eggs for verification.

It is the outcome of the long evolutionary history that is shared by African cuckoo and fork-tailed drongo. There is a major conflict between both bird species, because the brood parasite fully depends on the services of the foster parent, and the burden on the foster parent is enormous.

Arms race

It starts with the fact that an African cuckoo female destroys a drongo egg after arriving to lay an egg in the nest of a fork-tailed drongo couple. The cuckoo chick finishes the job. It hatches first and pushes the drongo eggs out of the nest; if a chick happens to have hatched already, it is also thrown out. The foster parents lose their entire clutch. And they are busy for weeks with the demanding care of the foster chick.

This conflict with major interests created an arms race. The drongo learned to recognize cuckoo’s eggs and to reject them. In response, the cuckoo developed eggs that increasingly resembled drongo eggs. Currently, the mimicry is almost perfect: in the eyes of drongos, cuckoo eggs look exactly like drongo eggs.

Individual signature

Drongo eggs are hugely variable. The background colour ranges from white to reddish brown, and the eggs can be immaculate, speckled, or blotched. Between eggs of the African cuckoo, the same variation exists. The mimicry is excellent on population level, and the African cuckoo seems to be ahead in the arms race.

But in reality, the fork-tailed drongo is the winner.

That is because a drongo female consistently produces eggs with the same look. Each female has her own characteristic colour and pattern. She puts, as it were, a distinctive signature on each egg for verification: I laid this one. A cuckoo female lays eggs that fall within the drongo variation, but she lays them randomly. Chances are small that she lays an egg in the nest of a drongo female that produces exactly the same egg type. The cuckoo egg usually is aberrant.

Protected

Conducting experiments and using models, the researchers predict how likely it is that a fork-tailed drongo will recognize and reject an egg of the African cuckoo in her nest. And that is more than 90 percent! Without individual egg signatures, that chance would be much smaller. So, the strategy of drongos – great variation between clutches, great uniformity within clutches – is an excellent response to the almost perfect mimicry of cuckoos, protecting the drongo effectively against the brood parasite.

And so, the African cuckoo has little success with this host. A cuckoo’s egg seldomly is accepted. If you consider that about one in five drongo nests is lost during breeding, the brood parasite has an extremely low reproductive success. But apparently, that low success is enough for the species to survive.

Willy van Strien

Photo: African cuckoo. Alastair Rae (Wikimedia Commons, Creative Commons CC BY-SA 2.0)

Sources:
Lund, J., T. Dixit, M.C. Attwood, S. Hamama, C. Moya, M. Stevens, G.A. Jamie & C.N. Spottiswoode, 2023. When perfection isn’t enough: host egg signatures are an effective defence against high-fidelity African cuckoo mimicry. Proceedings of the Royal Society B, online 26 July. Doi: 10.1098/rspb.2023.1125
Stoddard, M.C., R.M. Kilner & C. Town, 2014. Pattern recognition algorithm reveals how birds evolve individual egg pattern signatures. Nature Communications 5: 4117. Doi: 10.1038/ncomms5117

Fairy lantern rediscovered

15 March 2023 /

Unexpectedly, the cheating plant Thismia kobensis still exists

The rediscoverd Kobe fariry lantern is a cheater

It was discovered in 1992 and believed to be extinct because the site where it had been found was destroyed in 1999. But now, it is rediscovered elsewhere: the Kobe fairy lantern. Kenji Suetsugu and colleagues describe the beautiful but cheating tiny plant.

You would hardly recognize them as plants, the small, splendid ‘fairy lanterns’ on the forest floor, often hidden under fallen tree leaves. Fairy lanterns, Thismia species, are indeed remarkable plants. What you see are the flowers, less than a centimeter in size. The plants have no green leaves, only some scales on the very short stem. Most of the plants lives underground.

There are about 90 species, one of which is Thismia kobensis, the Kobe fairy lantern. Small and inconspicuous as it is, it was only discovered in 1992, in an oak forest near the Japanese city of Kobe. The find was small: it consisted of no more than one specimen. The site was destroyed in 1999 when an industrial complex was constructed, and the newly discovered species went extinct. That was what people thought. But fairy tales exist: in 2021 biologists unexpectedly rediscovered the plant on a conifer plantation in the town of Sanda, 30 kilometers from the original site. And this time the find was larger: almost 20 individuals. Now, Kenji Suetsugu and colleagues provide a scientific description of the species.

The loveliness of its flower is deceptive: Thismia kobensis belongs to a group of cheating plants.

Energy requirement

The cheating has to do with the lack of green leaves.

The green leaves of normal plants contain many chloroplasts. In these cellular organelles, photosynthesis takes place: plants extract carbon dioxide from the atmosphere and with the help of sunlight they fix the carbon in carbohydrates such as sugars and starch. From these carbohydrates, they derive energy. Plants without green leaves cannot make carbohydrates, but they do need energy.

Many of these plants solve this problem by extracting sugars with their roots from fungi in the soil. The scientific term for this is mycoheterotrophy.

Fairy lantern is sugar thief

Most mycoheterotrophic plants target fungi that live in a mutualistic relationship with green plants. The fungi get sugars from these plants. In return, the fungi help the green plants to absorb water and nutrients such as nitrogen and phosphorus from the soil. This collaboration, called mycorrhiza, is mutually beneficial and both parties are honest.

However, when mycoheterotrophic plants such as Thismia make contact with mycorrhizal fungi, they don’t cooperate in this way. They do receive water and nutrients, but they do not return sugars. They can’t. Instead, they take up sugars from the fungus in addition to water and nutrients. In other words: they steal. The fungus had received those sugars from green plants, so mycoheterotrophic plants indirectly parasitize on green plants via mycorrhizal fungi.

Difficult alternative

There are about 500 species of mycoheterotrophic plants. They live on nutrient-poor soils in forests, where little sunlight reaches the soil and the ability for photosynthesis, i.e., sugar production, is limited. Sugar theft is the alternative that these plants developed.

sarcodes sanguinea is a myceheterotrophic plantBut it’s not as easy as it seems. It is difficult for a mycoheterotrophic plant to form a relationship with a mycorrhizal fungus. Where a green plant interacts with many mycorrhizal fungi species simultaneously, a mycoheterotrophic plant can make contact with only one or a few fungal species. That’s probably because most fungi detect the cheaters and hold off on the relationship. Therefore, mycoheterotrophic plants are always rare and never widely distributed.

Mycoheterotrophic species often target a fungus that has many different green partners. With so many suppliers, the sugar supply is always guaranteed.

Dust seeds

The vast majority of land plants live in association with mycorrhizal fungi. The mycoheterotrophic mode of life -which abuses this mutualism – has developed dozens of times. In the case of fairy lanterns, this happened many millions of years ago. That is why they have little resemblance to ordinary plants. Other mycoheterotrophic plants emerged much more recently and have a more normal appearance.

the brid's nest is a mycoheterotrophic orchidSome plants are mycoheterotrophic shortly after germination only; this applies to all orchid species. The seeds are as fine as dust and contain no food. After germination, these plants get their sugars from fungi until they have leaves and can make their own sugars. This could be a first step towards a fully mycoheterotrophic lifestyle. There are also orchid species that stay mycoheterotrophic during their whole life, for example the bird’s nest, Neottia nidus-avis.

Broomrape species (Orobanche) look similar to some mycoheterotrophic plants, but are different: with their roots, they parasitize directly on other plants.

Willy van Strien

Photos:
Large:
Fairy lantern of Kobe, Thismia kobensis ©Kenji Suetsugu
Small:
Snow plant, Sarcodes sanguinea, a mycoheterotrophic plant from North-west America. David῀O (Wikimedia Commons, Creative Commons CC BY 2.0)
Bird’s nest orchid, Neottia nidus-avis. BerndH (Wikimedia Commons, Creative Commons CC BY-SA 3.0)

Sources:
Suetsugu, K., K. Yamana & H. Okada, 2023. Rediscovery of the presumably extinct fairy lantern Thismia kobensis (Thismiaceae) in Hyogo Prefecture, Japan, with discussions on its taxonomy, evolutionary history, and conservation. Phytotaxa 585: 102-112. Doi: 10.11646/phytotaxa.585.2.2
Gomes, S.I.F., M.A. Fortuna, J. Bascompte & V.S.F.T. Merckx, 2022. Mycoheterotrophic plants preferentially target arbuscular mycorrhizal fungi that are highly connected to autotrophic plants. New Phytologist 235: 2034-2045. Doi: 10.1111/nph.18310
Jacquemyn, H. & V.S.F.T. Merckx, 2019. Mycorrhizal symbioses and the evolution of trophic modes in plants. Journal of Ecology 107: 1567-1581. Doi: 10.1111/1365-2745.13165
Gomes, S.I.F., J. Aguirre-Gutiérrez, M.I. Bidartondo & V.S.F.T. Merckx, 2017. Arbuscular mycorrhizal interactions of mycoheterotrophic Thismia are more specialized than in autotrophic plants. New Phytologist 213: 1418-1427. Doi: 10.1111/nph.14249

Cuckoo duck seeks defence

10 October 2022 /

Foster family protects duck eggs against birds of prey

Cuckoo duck dumps its eggs in nest of aggressive host

Young cuckoo ducks do not need any care: they are independent upon hatching. Then why does the duck burden other birds with its eggs, Bruce Lyon and colleagues wondered.

In South America a duck species occurs that, like a cuckoo, lays its eggs in nests of other bird species. The hosts then unintentionally take care of them. This is the black-headed duck, Heteronetta atricapilla, with the appropriate nickname cuckoo duck; it is a so-called brood parasite.

Bruce Lyon and colleagues wondered why the cuckoo duck dumps its eggs in other birds’ nests. They don’t require much care, apart from brooding. After hatching, the young are immediately independent. That is a big difference with all other brood parasites, such as the common cuckoo. These species have young that have to be fed and protected for weeks, so it is very profitable for parents to outsource the care. But how does the cuckoo duck profit?

Easy prey

The shedding of parental duties may have to do with the danger of predation, Lyon hypothesized. If the cuckoo duck were to make its own nest, it would be close to water. And in such nest, eggs are easy prey for avian predators, especially the chimango caracara. This was shown in experiments in which the researchers placed chicken eggs in a self-made, unguarded nest. Within a few days, all eggs were gone.

Unless they placed the nest in a colony of brown-headed gulls. In that case, hardly any egg was stolen.

This gull is one of the hosts in whose nests the cuckoo duck dumps its eggs. In Argentina, where the study was conducted, two other important hosts occur, the red-fronted coot and the red-gartered coot. Like the brown-headed gull, they are aggressive birds that are capable to defend their nests fiercely. Is that the reason why the cuckoo duck chooses them to care for its offspring?

Safe

It seems to be. The duck eggs are indeed quite safe with these fierce foster parents, the researchers noted. Admittedly, it may happen that foster parents recognize a foreign egg and throw it out of the nest. But if they accept the egg, it almost always remains undisturbed and hatches. This very high chance of survival upon acceptance far outweighs the risk of rejection.

The researchers do not know exactly how much the cuckoo duck gains. They could not determine how many eggs would survive in a self-defended nest, because it never builds a nest. But related duck species that do incubate and guard their own eggs lose quite a lot to birds of prey.

Willy van Strien

Photo: black-headed duck couple. Cláudio Dias Timm (Wikimedia Commons, Creative Commons BY-SA 2.0).

Source:
Lyon, B.E., A. Carminati, G. Goggin & J.M. Eadie, 2022. Did extreme nest predation favor the evolution of obligate brood parasitism in a duck? Ecology and Evolution 12: e9251. Doi: 10.1002/ece3.9251

Increasing efficiency in brood parasite

12 April 2022 /

Cuckoo catfish improves its timing

Cuckoo catfish, Synodontis multipunctatus, improves efficiency by practizing

It is not easy for a cuckoo catfish to get its eggs adopted by intended host parents, because these are wary. But it learns the trick by experience, as Holger Zimmermann and colleagues show.

Cuckoo catfish dump their eggs at host parents to let them take care of their offspring: they are brood parasites. That seems easy and, in a way, it is, because the eggs can develop safely without the real parents having to worry. But they do have to bring them to the host parents, and that is not so easy. In that sense, cuckoo catfish spend more effort for their offspring than most fish, which simply lay eggs and leave them behind.

They have to practice the art of parasitism, Holger Zimmermann and colleagues write. The cuckoo catfish (Synodontis multipunctatus) is, as far as we know, the only fish species that, like a cuckoo, relegates the raising of its offspring to others. It lives in Lake Tanganyika in Africa.

Abuse

It takes advantage of species of cichlids that have the most extensive form of parental care, the so-called mouthbrooders. In these species, mothers take the fertilized eggs in the mouth and keep them there until they hatch, after a few weeks.

During spawning, such mouthbrooding cichlids circle around each other and release eggs and sperm; in between acts, they defend the spawning site against intruders.

But a group of cuckoo catfish may intrude. They consume some cichlid eggs before the mother has been able to collect them and drop a few eggs themselves and fertilize them. The cichlid mother panics and collects her eggs as fast as she can; in her haste, she also takes up catfish eggs.

The catfish must interfere at exactly the right time, when the female cichlid is busy laying eggs; it’s a matter of seconds. By experience, they learn to improve the timing of egg laying and fertilization, Zimmermann shows with experiments in tanks, in which he exposed cichlids (4 males and 12 females) to three cuckoo catfish pairs.

Sharper timing

The researchers searched for host parents that have no resistance against the underwater cuckoo. With resilient host parents, the learning process of the parasite would not show up. They selected the mouthbrooder Astatotilapia burtoni, which lives in Lake Tanganyika and is known to the catfish. But they took a population from a neighbouring river, where the cuckoo catfish does not occur. The chosen host parents have no innate defences against cuckoo catfish, nor do they learn to avoid it, but they do behave aggressively towards any fish that disturb the spawning to predate on eggs.

Unexperienced cuckoo catfish almost never managed to get their eggs taken up by these host parents. Only 3 percent of their attempts succeeded. But after some time – in the experiments after four months, about 30 attempts – things got much better: more than 25 percent of the attempts now was successful. That success rate did not increase further. Experienced catfish also managed to consume more eggs of the host parents in the brief time available.

The improvement was possible because the parasites learn to lay and fertilize their eggs at precisely the right time, as behavioural observations showed. In addition, groups of catfish improve the coordination of their intrusive act.

Host parent is loser

Most attempts fail, though, even in experienced cuckoo catfish, because the vigilant cichlids outsmart their enemy. But that does not matter, because the profits for the parasite are large if the action does succeed. A host mother then carries on average five parasite eggs. The catfish will hatch sooner than the cichlids, and the young catfish devour some cichlid embryos.

The host mother is the loser. She is abused and produces fewer young of her own.

Willy van Strien

Photo: Cuckoo catfish. Calwhiz. (Via Flickr, CC BY-NC-ND 2.0)

Cichlids from Lake Tanganyika have learned to coexist with cuckoo catfish

Source:
Zimmermann, H., R. Blažek, M. Polačik & M. Reichard, 2022. Individual experience as a key to success for the cuckoo catfish brood parasitism. Nature Communications 13: 1723. Doi: 10.1038/s41467-022-29417-y

New body

17 March 2021 /

Loose head regenerates a complete Elysia sea slug

Elysia sea slug can grow new body from head

Sea slugs Elysia marginata en Elysia atroviridis can decapitate themselves and regrow a new body from the loose head, Sayaka Mitoh en Yoichi Yusa show. A bizarre phenomenon. Why do they do it, and how do they survive?

Sayaka Mitoh and Yoichi Yusa must have been dumbfounded when seeing sea slugs that they kept in their lab, species Elysia marginata, sever their heads from their bodies. The loose heads moved around, as they report. After a day, the wounds were closed. In some cases, especially in young sea slugs, things got even crazier: the head began to feed; after a week, a new body started to grow and in three weeks it was complete.

The loose bodies also moved for a while, sometimes even months, but eventually they decomposed. No new head appeared on any loose body.

Parasite

There are more animals that can regrow a missing body part, such as a lizard that shed its tail or a fiddle crab that lost a claw. But this – regenerating almost an entire body – is very extreme. These sea slugs even have a groove behind the head as a predetermined breakage plane for self-decapitation. Why do they do it?

In any case, it is not to escape from a predator, like a lizard sheds its tail when a predator grasps it. The sea slugs take hours to separate body from head; that is not effective to avoid predation. And when the researchers simulated an attack by teasing them, nothing happened. The animals have a different defence mechanism against predators: they are poisonous.

The reason for self-decapitation became clear by observations on wild-caught specimens of a related species, Elysia atroviridis. Once in the lab, some of them shed the whole body, and these specimens turned out to contain a parasite, a copepod of the genus Arthurius. It is a large parasite that occupies almost the entire body of its host. In fact, a parasitized sea slug has already lost its body. If it sheds it, it will get rid of the parasite while losing almost nothing more.

Chloroplasts

But how does it survive without organs such as heart and kidneys? This has to do with a special property of sacoglossan sea slugs, to which Elysia belongs, the researchers suppose. They extract chloroplasts from algal food and incorporate them in special cells that line their highly branched digestive gland. The head also contains chloroplasts. Thanks to the chloroplasts, which they need to survive, these sea slugs can endure a period without food, it was known.

It is a mystery how exactly they utilise the chloroplasts. The chloroplasts continue to do what they do in plants: they convert carbon dioxide into carbohydrates with the help of sunlight, a process called photosynthesis. Whether the sea slugs can survive on sunlight as a result, just like plants, is a matter of debate.

Regardless, it may well be thanks to the chloroplasts that a loose head of Elysia marginata and Elysia atroviridis survives.

No eternal life

Parasitized Elysia sea slugs shed their worthless bodies. But they only manage to grow a new one from the head when they are young. The loose head of an older specimen does not feed and does not grow, but will die within ten days. Shedding and regrowing a body is not a recipe for eternal life.

Willy van Strien

Photo: Elysia marginata. Budak (via Flickr, CC BY-NC-ND 2.0)

The research explained on YouTube

Sources:
Mitoh, S. & Y. Yusa, 2021. Extreme autotomy and whole-body regeneration in photosynthetic sea slugs. Current Biology 31: R233-R234. Doi: 10.1016/j.cub.2021.01.014
Wägele, H., 2015. Photosynthesis and the role of plastids (kleptoplastids) in Sacoglossa (Heterobranchia, Gastropoda): a short review. Aquatic Science & Management 3: 1-7. Doi: 10.35800/jasm.3.1.2015.12431

Well-timed flowering

10 September 2020 /

Dodder eavesdrops on host plant’s signal

dodder manages to flower simultaneously with its host

Dodder, a plant that parasitizes other plants, flowers almost simultaneously with its host. The parasite takes up the host’s signal that activates flower development, Guojing Shen and colleagues show.

A plant may be covered with a tangle of thin, sticking threads. That is a bad condition for the plant, because those threads are stems of a parasitic plant: dodder (Cuscuta), of which about two hundred species exist worldwide. Most of them thrive on several host plant species. And whether a host flowers sooner or later in the season, dodder joins in and develops its flowers simultaneously. Guojing Shen and colleagues discovered how Australian dodder (Cuscuta australis) manages to synchronize its flowering time with that of its various hosts.

Once young dodder plants get hold of a host plant after germination, their roots disappear, so they cannot take up water and nutrients from the soil anymore. Also, they don’t have green leaves that take carbon dioxide from the air and convert it into carbohydrates with the help of sunlight, like other plants. Everything they need, they extract from the host, round the stems of which they wind extensively.

Maximum benefit

To exploit its host, the parasite forms numerous haustoria that penetrate into the host’s stems and connect with phloem, the tissue that transports organic compounds, and xylem, the tissue that transports water. The haustoria enable the parasite to extract nutrients and water from its victim.

Annual dodder species, like Cuscuta australis, first grow, then flower and eventually die. The parasite benefits most from its host when it flowers simultaneously. Because if it blooms earlier, it will not reach the size it could have reached by growing longer, and as a consequence it will produce fewer flowers and fewer seeds than it could have produced. But if it postpones flower development for too long, it will be short of nutrients during flowering. Because the host then channels as much nutrients as possible to its own flowers and seeds, leaving less to circulate in phloem and xylem from which dodder taps.

So, dodder has to adjust its flowering time to that of its host.

Dodder is eavesdropping

Most plants regulate their flowering time by tracking changes in day length. When it is about time for flowers to appear, the leaves produce the protein FT (flowering locus T), which moves through the phloem. This protein switches on flower development; it is, in other words, a mobile flowering signal.

Dodder would not benefit from having a flowering signal of its own. As it has to synchronize with its host, it must be flexible. It is therefore not surprising that it does not appear to have functional FT protein. There is a dodder variant of the protein, but it does not activate flowering. How then does the parasite regulate its flowering time?

By eavesdropping on the host’s flowering signal, Shen writes. He investigated flowering in Australian dodder, but the story will apply to other dodder species as well. To European dodder (Cuscuta europaea), for example, which can be found in Western Europe growing on nettle and hops; or to lesser dodder (Cuscuta epithymum), or hellweed, that grows on heather, broom, gorse, thyme and other plants.

It was already known that the parasite not only extracts water and nutrients from the host plant via haustoria, but that also several biologically active substances are exchanged.

Including the FT protein.

Perfect mechanism

As the host starts flower development and the plant produces FT protein, this is transferred to dodder. The researchers show that the host’s protein retains it activity in the parasite, initiating flower development there too.

And so the flowering time of the parasite will coincide nicely with that of its host. Eavesdropping is a perfect method for alignment.

Willy van Strien

Photo: Australian dodder, Cuscuta australis. Harry Rose (Wikimedia Commons, Creative Commons CC BY 2.0)

Watch the growth of fiveangled dodder (Cuscuta pentagona, from North America) on video

Sources:
Shen, G., N. Liu, J. Zhang, Y. Xu, I.T. Baldwin & J. Wu, 2020. Cuscuta australis (dodder) parasite eavesdrops on the host plants’ FT signals to flower. Proceedings of the National Academy of Sciences, online August 31. Doi: 10.1073/pnas.2009445117
Liu, N., G. Shen, Y. Xu, H. Liu, J. Zhang, S. Li, J. Li, C. Zhang, J. Qi, L. Wang & J. Wu, 2020. Extensive inter-plant protein transfer between Cuscuta parasites and their host plants. Molecular Plant 13, 573-585. Doi: 10.1016/j.molp.2019.12.002

Males parasitizing on females

13 August 2020 /

The immune system of deep-sea anglerfishes is strongly modified

In deep-sea anglerfish, some species have parasitic males and an aberrant immune system

To the well-known peculiarities of deep-sea anglerfish, Jeremy Swann and colleagues add a new one: some species lack an important part of the immune system. This is associated with a unique parasitic lifestyle of males.

There are strange, very strange and extremely weird animals. We can safely include deep-sea anglerfish in the latter group.

Within the anglerfish or seadevils, they form a separate group of over 160 species, the Ceratioidea, which, as the name indicates, have specialized in living in the utter darkness of the deep sea. Food and partners are extremely scarce down there. Hence, as was known, these fish exhibit some peculiarities. Now, it turns out that they also have a very aberrant immune system, Jeremy Swann and colleagues report.

Angling pole with glowing bulb

Deep sea anglerfish start their lives in a quite normal way, eggs and larvae dwelling in surface waters. But once they developed into young fish, things change. Females grow to a considerable size, males stay tiny.

The bigger a female gets, the more eggs she can produce. And so a young female starts growing. She has to eat much, several prey animals are on her menu. To capture prey, she uses a fishing rod growing from her back; it is a modified anterior dorsal fin. At the end it has a lure: a bulb in which bacteria live that produce light by carrying out a chemical reaction. It is a form of mutualism; the bacteria get a place to live in and food in exchange for light production.

An anglerfish’s light can flash and dance, resembling a moving animal. Living animals discern a tasty snack which they will approach. The anglerfish then ingests a large amount of water, including prey. With some luck, the catch will provide sufficient nutrients to sustain her for quite a while.

The females, plump and with large heads and mouths full of sharp teeth, are not the prettiest of all. They are called seadevils for good reason. They are bad swimmers, drifting around, just waiting for prey to come by.

Strong attachment

After completing the larval stage, males’ development takes a completely different direction. Males no longer grow and are unable to eat. Their only goal is to find a female in the empty deep sea. So, they swim constantly. In addition to the light bulb of their angling rod, young females also have two luminous organs on their backs. Maybe the dwarfed males, which have big eyes, are able to detect those organs. If they are lucky, they will meet a partner before they have used up all their reserves.

Upon meeting, he attaches himself to her body with sharp teeth. When, later on, she is ready to release eggs, he is ready to fertilize them. Males and females only become sexually mature when they’ve acquired a partner. Given the scarcity of conspecifics, this makes sense: only after pair formation it is guaranteed that eggs and sperm can come into contact.

Sperm bulge

In some deep-sea anglerfish, the attachment between female and male is temporary; after a while, he lets go.

But in other species, males attach themselves permanently to a female. These are most bizarre types, because the two partners fuse with each other, enabling the male to survive. Their skin tissues meld, the circulatory systems become connected. He now is a ‘sexual parasite’, little more than a sperm-producing bulge that feeds on nutrients that he derives from her. This sexual parasitism is a unique mode of reproduction, occurring only in deep-sea anglerfish.

It is called parasitism, but it may be considered a form of mutualism as well, as the male delivers sperm in return for nutrients.

The best known species is Ceratias holboelli; it is also the largest one and it has the most extreme sexual dimorphism. A female can grow more than a meter long (including tail), sixty times the size of a free-living male. Physical pair formation is permanent. Once attached to her belly, he grows to a maximum of 20 centimetres. A female carries no more than one parasitic male.

Another species with permanent attachment is Cryptopsaras couesii; in this species, up to eight males can be attached to a single female. A female can be 30 centimetres long, a free-living male only three centimetres.

Ancient immune system

It is remarkable that the female immune system doesn’t attack permanently attached, parasitic males, Swann and colleagues realized. You would expect the immune system to recognize and reject such males, as they are not-own tissue. But that does not happen.

Apparently, the immune system tolerates the very intimate mode of reproduction. To find out how, the biologists examined a number of genes that underpin various parts of immune defence. They investigated four deep-sea anglerfish species with temporarily attached males and six species with permanently attached parasitic males, including Cryptopsaras couesii. They compared these species to a number of anglerfish species outside the deep-sea group, where males don’t attach to females.

Fishes have the same immune system as other vertebrates; the system is 500 million years old. It consists of innate, general immune responses on the one hand and specific immune responses that build up against specific intruders that the system has to deal with on the other hand. The researchers focused on the adaptive, specific immune system.

Lethal

The results were surprising: deep sea anglerfish species in which males live as parasites on females lack essential immune genes. Their specific immune system is severely blunted.

In two of the species studied, species in which females can have more than one male attached, virtually no specific immune facilities are functional. This is highly remarkable, because such complete lack of specific immune defence is lethal for other animals. The first infection would kill them. Microbial pathogens occur in the deep sea too, so deep-sea anglerfish must be able to defend themselves. Most likely, they reorganized their innate immune defence, the researchers assume.

From their own and other research, they conclude that the common ancestor of deep-sea anglerfish had tiny, non-parasitic males that temporarily attached themselves to females. On a few occasions, species descending from that ancestor made the switch to permanent attachment and their specific immune defence has been largely dismantled.

It is unclear yet what happened first. Did males become parasitic, making it necessary to turn off the specific immune system? Or did the specific immune system lose important parts, making permanent attachment of males possible?

The deep sea anglerfish remain really puzzling creatures.

Willy van Strien

Drawing: northern giant seadevil, Cryptopsaras couesii (not included in this research); female with male attached. Tony Ayling (Wikimedia Commons, Creative Commons CC BY-SA 1.0)

Watch the fanfin angler, Caulophryne jordani (not included in the research) on YouTube; female with permanently attached male

Sources:
Swann, J.B., S.J. Holland, M. Petersen, T.W. Pietsch, T. Boehm, 2020.  The immunogenetics of sexual parasitism. Science, online July 30. Doi: 10.1126/science.aaz9445
Fairbairn, D.J., 2013. Odd couples. Extraordinary differences between the sexes in the animal kingdom.  Princeton University Press, Princeton and Oxford, VS. ISBN 978-0-691-14196-1

Resemblance is striking

5 August 2020 /

Parasitic Vidua nestlings trick host parents with near-perfect mimicry

Vidua nestlings mimic the young of their host parents

In order not to stand out in the nest in which they grow up clandestinely, Vidua nestlings mimic the young of the host parents. They perform very well, Gabriel Jamie and colleagues report. But some slight discrepancies exist.

African whydahs and indigobirds, Vidua species, are brood parasites like the cuckoo. They lay their eggs in the nest of other bird species, in this case grassfinches, and have the host parents raise their young. Vidua finches are unable to provide parental care. But these brood parasites do much less harm to the host families than a cuckoo, because young Viduas don’t eject other nestlings from the nest. The host parents take care for their own offspring, but have some extra, foreign young.

The foreign nestlings should not stand out, otherwise the tricked parents will notice the deception. It was already known that Vidua young resemble their host parents’ young. With special computer software, Gabriel Jamie and colleagues now show how successful the mimicry is.

Ornamented mouths

pin-tailed whydah is brood parasiteThe Vidua genus contains nineteen species. In the breeding period, the males are real beauties, while the females are inconspicuous and difficult to recognize. Jamie took a closer look at three species: pin-tailed whydah (Vidua macroura), broad-tailed paradise whydah (Vidua obtusa) and purple indigobird (Vidua purpurascens). They are host-specific, each Vidua species has a single host species. Jamie compared the Vidua nestlings to that of their respective host parents and of a number of other grassfinch species.

Young grassfinches (Estrildidae) have ornamental mouth markings that become fully visible when they open their beaks; this ornamentation in unusual among birds. Each grassfinch species has its characteristic pattern, colour and structure.

Nestlings of the breeding parasites accurately mimic those characteristic markings, is the conclusion of the research. An analysis with pattern recognition software shows that the pattern is similar to that of their host parent species. The colours match well too. Vidua nestlings also cleverly imitate the begging calls and postures of their foster siblings.

Imprinting

Previous research, by Michael Sorenson, had shown that the nineteen species of whydahs and indigobirds are much younger than their hosts in an evolutionary sense. The idea is that their common ancestor switched to a brood parasitic lifestyle with a grassfinch as host parent.

Speciation could then occur quickly. Whenever a Vidua female happens to lay eggs in the nest of another host, a separate group associated to that new host arises, because Vidua nestlings imprint on the song of their host father. Each grassfinch species has its own characteristic song. When grown up, Vidua males will mimic the song of their host, and females are attracted to this song. Also, females select a nest of the host species they were raised by to lay their eggs in. The group turns into a new species.

The nestlings then become more and more similar to the nestlings of the new host through an evolutionary adaptation process. Because the more a Vidua nestling resembles the young of its host parents, the more likely they are to accept it and care for it, increasing its survival chance.

Exaggerated

And as a matter of fact, the resemblance between foreign and own young in a parasitized grassfinch’s nest turned out to be striking. But it is not entirely perfect. Small but consistent differences exist. Perhaps the foreign nestlings are (yet) unable to fully mimic their nest mates. And apparently, they are doing well enough: the host parents accept them.

But there may be another explanation for the discrepancies, the researchers write. Nestlings of pin-tailed whydah, for example, have spots in the beak that are slightly larger than those of their foster parents’ young, common waxbill (Estrilda astrild), and their begging calls are slightly extended. Unlike a waxbill nestling, they wave a wing under their open mouth while begging.

So, these Vidua nestlings are slightly exaggerating their host’s begging signals. And perhaps the host parents favour them as a consequence. An intriguing thought.

Willy van Strien

Photos:
Large: pin-tailed whydah nestling, the outside of the mouth markings visible. ©Gabriel A. Jamie
Small: pin-tailed whydah, breeding male. Alan Manson (Wikimedia Commons, Creative Commons CC BY-SA 2.0)

Sources:
Jamie, G.A., S.M. Van Belleghem, B.G. Hogan, S. Hamama, C. Moya, J. Troscianko, M.C. Stoddard, R.M. Kilner & C.N. Spottiswoode, 2020. Multimodal mimicry of hosts in a radiation of parasitic finches. Evolution, online July 21. Doi: 10.1111/evo.14057
Sorenson, M.D., K.M. Sefc & R.B. Payne, 2003. Speciation by host switch in brood parasitic indigobirds. Nature 424: 928-931. Doi: 10.1038/nature01863

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