From so simple a beginning

Evolution and Biodiversity

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Perfume makers

Male orchid bees concoct a precious perfume

A beautiful colour with a metallic sheen appears to be insufficient for male orchid bees to impress females. They must also have an attractive scent. Orchid bees (Euglossini, about two hundred species) are found in tropical America. They do not live in colonies, like the honeybee. Males occupy a territory and try to attract females.

A wonderful smell is provided by a self-made perfume, which consists of a mixture of scents that males collected from flowers, rotting wood, sap from trees and – weird enough – faeces. Males differ in the intensity and complexity of their perfume, and only a few males have an outstanding blend. That’s no wonder, because it takes a lot of time and energy to find and collect the dozens of aromatic components, most of which are scarce. Young bees in particular work fanatically to concoct their perfume, as Jonas Henske and Thomas Eltz discovered during their research on Euglossa imperialis in Costa Rica. Males of this species can live for six weeks to three months.

Hundreds of species of orchids benefit from the male orchid bees’ urge to collect scents. They are pollinated exclusively by these bees, in exchange for a precious fragrance.

Males capture volatile odours by spitting lipids onto a sweet-smelling surface. The fragrances are absorbed by the lipids. The bees then use their legs to stuff the scented fat into special pouches on their hind legs. They regularly take out the content to enrich it with new odours, creating an extensive and complex mixture of fragrances.

A male that wants to mate makes hovering flights in his territory, moving his legs in a characteristic way. Underneath its body, the right and left middle legs alternately sweep the pouches of the opposite hind leg. Tufts of hair on the middle legs absorb some fat. The fluttering wings then spread the perfume that is released.

Experiments in the lab showed that females are interested. The perfume allows them to determine whether they are dealing with a male of their own species; each species of orchid bee has its characteristic scent bouquet. The species Euglossa dilemma and Euglossa viridissima, for example, look similar, but can be distinguished by smell. This indicates that the males carefully compose their scent mixture: all components in exactly the right proportions.

The researchers had assumed that the oldest male orchid bees would have the largest supply and the most complex perfume, because they had had the most time to create it. Such a precious perfume would be evidence that its owners had lived a long time, a signal of good hereditary quality and good condition. But that idea turns out to be wrong.

To test their assumption, Henske and Eltz attracted Euglossa imperialis males, captured them, estimated their age, and sealed the perfume pouch on the right hind leg with glue. They then released the animals and waited for them to reappear at the original capture site. Half of the males returned within five days, some stayed away for more than twelve days. The researchers could capture about a third for the second time, and then they compared the contents of both perfume pouches.

Between the first and second measurement, young males had improved the perfume in the pouch on the left hind leg, which had been left open: the supply had become larger, and the perfume had a more varied composition than that in the sealed right pouch. The perfume in the left pouch of old males had deteriorated in quantity and quality.

Perhaps young orchid bee males have a sharper sense of smell, or are more efficient at finding and storing odours, the researchers think. But it may also be a trade-off. Males collect scents and court females throughout their lives, expanding their perfume supply continuously on the one hand and using bits of it up on the other. The balance can change. For males that do not have much time left to live, it may not be worth acquiring more scent; they better use the perfume supply they have.

Unfortunately, it is not known whether females prefer a more complex scent.

Willy van Strien

Photo: Euglossa species male. Thomas Shahan (Wikimedia Commons, Creative Commons BB BY 2.0)

Sources:
Henske, J. & T. Eltz, 2024. Age-dependent perfume development in male orchid bees, Euglossa imperialis. Journal of Experimental Biology 227: jeb246995. Doi: 10.1242/jeb.246995
Eltz, T., C. Bause, K. Hund, J.J.G. Quezada-Euan & T. Pokorny, 2015. Correlates of perfume load in male orchid bees. Chemoecology 25:193-199. Doi: 10.1007/s00049-015-0190-9
Eltz. T., Y. Zimmermann, J. Haftmann, R. Twele, W. Francke, J.J.G. Quezada-Euan & K. Lunau, 2007. Enfleurage, lipid recycling and the origin of perfume collection in orchid bees. Proc. R. Soc. B 274: 2843-2848. Doi: 10.1098/rspb.2007.0727
Eltz, T., D.W. Roubik & M.W. Whitten, 2003. Fragrances, male display and mating behaviour of Euglossa hemichlora: a flight cage experiment. Physiological Entomology 28: 251-260. Doi: 10.1111/j.1365-3032.2003.00340.x

Suckling amphibian

Ringed caecilian feeds milk to her young

Mammals suckle their young. This behaviour distinguishes them from other vertebrates: fish, amphibians, reptiles, and birds. Yet that distinction is not watertight, as a few bird species exist that produce a kind of milk to feed their young: some pigeons and doves, some flamingos, and the emperor penguin. And now, Pedro Mailho-Fontana and colleagues report that females of the ringed caecilian, an amphibian, feed their young with something that resembles mammalian milk. Thanks to this ‘milk’, the youngsters grow rapidly.

It is not surprising that this peculiar trait, which is easily observable, is only now coming to light. The biology of caecilians is poorly known because the animals live underground. Caecilians (Gymnophiona) form a third group within the amphibians, next to frogs & toads and salamanders. They have no legs, have reduced eyes, and are blind; they have two tentacles with which they find their way underground.

The caecilian in question here is the ringed caecilian (Siphonops annulatus). It is widespread in South America. The animal grows to over forty centimetres in length. A female lays eggs, on average ten at a time, in an underground round nest chamber. She is a devoted mother: she lays coiled up with the eggs on her body, and when the young have hatched, she stays with them for another two months; then the young are independent. Until that moment, she will not even leave for a brief time to find food for herself.

A female changes colour when she is attending hatchlings. Normally, ringed caecilians are bluish grey, but a mother turns whitish grey. It was already known that this colour is caused by fat droplets accumulating in her epidermis. Every few days, the young are allowed to scrape off that skin; for this purpose, they have spoon-shaped teeth in the lower jaw. They all do at the same time, ferociously; within ten minutes it is over, and peace returns until the mother’s skin is ready for consumption again. This ‘skin feeding’ occurs in more caecilian species.

But ringed caecilians hatchlings also get other food, Mailho-Fontana discovered: milk. He kept a number of animals in the lab and filmed their behaviour.

Hatchlings often assemble near their mother’s rear end, he observed. Further research revealed that glands in the mother’s oviduct walls produce a white, viscous fluid that emerges through the genital opening, the cloaca, several times a day. The stuff is rich in fats and carbohydrates.

The young imbibe it voraciously. This ‘milk’ is a more important source of nutrition than the mother’s skin, and it is thanks to the milk that the young grow very fast, the researchers think. Their weight doubles within a week after hatching. The mother, eating nothing, loses a third of her weight.

The mother releases milk when hatchlings touch her tail, often producing high-pitched sounds, which probably is begging behaviour. She then raises her body end vertically, and the hatchlings compete for a good place. On average, three of them drink at the same time until they are fully satiated.

Viviparous caecilian species in which the young drink milk in the oviducts before birth were already known. The discovery of oviductal milk in the egg-laying ringed caecilian was unexpected.

Willy van Strien

Photo: Ringed caecilian, female with young. ©Carlos Jared

Sources:
Mailho-Fontana, P.L., M.M. Antoniazzi, G.R. Coelho, D.C. Pimenta, L.P. Fernandes, A. Kupfer, E.D. Brodie Jr. & C. Jared, 2024. Milk provisioning in oviparous caecilian amphibians. Science 383: 1092-1095. Doi: 10.1126/science.adi5379
Jared, C., P.L. Mailho-Fontana, S.G.S. Jared, A. Kupfer, J.H.C. Delabie, M. Wilkinson & M.M. Antoniazzi, 2019. Life history and reproduction of the neotropical caecilian Siphonops annulatus (Amphibia, Gymnophiona, Siphonopidae), with special emphasis on parental care. Acta Zoologica. 100: 292-302. Doi: 10.1111/azo.12254
Wilkinson, M., A. Kupfer, R. Marques-Porto, H. Jeffkins, M.M. Antoniazzi & C. Jared, 2008. One hundred million years of skin feeding? Extended parental care in a Neotropical caecilian (Amphibia: Gymnophiona). Biology Letters 4: 358-361. Doi: 10.1098/rsbl.2008.0217

Repurposed

Tree fern Cyathea rojasiana transforms dead leaves into roots

The tree fern Cyathea rojasiana, which grows in Panama, has a crown of leaves on a trunk. Sometimes a new frond sprouts, sometimes an old leaf dies. But dying is not the end for a leaf, James Dalling and colleagues discovered: the decayed leaf gets a second life. At least: the rachis.

The tree fern grows to a height of two meters, the leaves are more than two meters long. A senescent leaf will bend down, the leaf tip touching the ground. The leaf rots away, but the rachis remains. A tree can have a ‘skirt’ of twenty to thirty of those remains. They look lifeless, but when Dalling tried to remove them, they were found to be firmly stuck in the ground.

Vascular bundles run through the rachis of a green leaf, transporting water and nutrients absorbed by the roots to the leaf tissue. These vascular bundles appear to be intact in the ground-stuck leaf remains of Cyathea rojasiana. They are surrounded by a black layer that apparently protects them from rotting. And, surprisingly, at the end, i.e., in the soil, a bunch of finely branched roots has sprouted from each vascular bundle.

The conclusion is that the former leaf rachises have been transformed into roots, in which the direction of the water flow is reversed: in green leaves, it flowed from stem to leaf tip, now it is from leaf tip to stem.

Cyathea rojasiana grows in wet, extremely nutrient-poor soil. Extra roots are not so much useful to absorb water, the researchers think, but to extract nutrients from a larger area of soil. They showed that the new roots indeed absorb nitrogen and transport it upwards.

For many plant species holds: you can stick a piece of stem or leaf in the ground, and roots will grow. But converting a leaf rachis into a root is something that, as far as we know, only Cyathea rojasiana does.

Willy van Strien

Photo: Tree fern Cyathea rojasiana with decayed leaves, now functioning as roots. ©James Dalling

James Dalling tells about his discovery on YouTube

Source:
Dalling, J.W., E. Garcia, C. Espinosa, C. Pizano. A. Ferrer & J.L. Viana, 2024. Zombie leaves: novel repurposing of senescent fronds in the tree fern Cyathea rojasiana in a tropical montane forest. Ecology e4248, 18 January online. Doi: 10.1002/ecy.4248

Sacrificing sleep

Male dusky antechinus reduces sleep in mating season

As for all species, producing as many offspring as possible is what life is all about for the dusky antechinus, Antechinus swainsonii. For males, which do not care for young, this means that they have to mate with as many females as possible, because every successful mating may increase the number of young they sire. To achieve this, only three weeks are available, because this is the period in which all females are fertile. Males experience fierce competition; as a consequence of the pressure to face this, they are twice as heavy as females.

This short and intensive mating season has a very bizarre ending for males: they all die. Females, that carry the young in a flap of skin (they have no complete pouch), stay alive and many of them experience a second reproduction season the next year. But for males, it is over after one time.

To score as many partners as possible in that single mating season, males cut back on rest, Erika Zaid and colleagues discovered.

The dusky antechinus, a species of broad-footed marsupial mice, is an insectivorous predator that lives in Australia. Before the mating season, male and female sleep an average of more than 15 hours per day. During the mating season, measurements of physical activity and EEGs show that males reduce this to 12 hours on average: 20 percent less. The increased activity, which they exhibit especially at night, is accompanied by a higher level of the male sex hormone testosterone in the blood, giving them extra time and strength to find females and get access.

Unfortunately, the researchers do not know whether males that sacrifice much sleep actually father more offspring. Also, they did not investigate whether males compensate for the lack of sleep by sleeping more deeply.

Sleeping less jeopardizes health. The concentration of corticosteroids, which suppress the immune system, increases, with ultimately fatal consequences. But because males will die soon anyway, staying healthy is no longer important. Mating more often is now a better strategy than getting enough sleep.

You might think that dusky antechinus males die after the mating season because they have been acting so unhealthy. But that is not how it works, according to the researchers. Their death is a certainty. The increase in corticosteroids hardly contributes anything to this fate, but it does ensure that they can sustain their increased activity.

Willy van Strien

Photo: Antechinus swainsonii. Catching the eye (Wikimedia Commons, Creative Commons CC BY 2.0)

Source:
Zaid, E., F.W. Rainsford, R.D. Johnsson, M. Valcu, A.L. Vyssotski, P. Meerlo & J.A. Lesku, 2024. Semelparous marsupials reduce sleep for seks. Current Biology, January 25 online. Doi: 10.1016/j.cub.2023.12.064

Coordinated rolling

Dung ball roller Sisyphus schaefferi: male pulling and female pushing dung ball

Dung ball rollers (Sisyphus species) have a striking habit. The dung beetles form pairs, take a piece of mammal droppings, construct a ball larger than themselves and roll it away in a straight line to make sure not to collide with other pairs that have taken a part of the same dung pile. When, often after demanding work, they arrive at a suitable place, they bury their ball in the soil together with an egg. The larva that will hatch from the egg is surrounded by excellent food.

Claudia Tocco and colleagues wanted to know more about the harmonious cooperation that male and female exhibit. They investigated how partners divide tasks in two species: Sisyphus fasciculatus from South Africa and Sisyphus schaefferi, that lives in North Africa, Southern Europe, and Asia Minor. In an outdoor test setup, they offered cow dung to groups of dung ball rollers. The beetles formed pairs, constructed a dung ball and started rolling.

The male, which is slightly larger than the female, is always the one driving the dung ball transport, as the researchers saw. He determines the course. He walks backwards and pulls the dung ball with his front legs. His partner walks on the other side, also backwards, with her head down and her hind legs on the ball. On flat terrain, she contributes nothing. If the male stops rolling, she also stops. So, you never see a female dragging a dung ball by herself. Conversely: if she stops, he goes on alone, rolling the dung ball as quickly and staying on course as well as a couple.

Mostly, she does move along, maintaining contact with the ball. Consequently, she can help immediately when things get difficult. And they do, because Sisyphus fasciculatus and Sisyphus schaefferi live in woodlands and forests, with all kinds of objects lying on the ground. A couple of dung ball rollers often encounters obstacles. The researchers conducted experiments to simulate these situations to see how the pair cleared them.

First, they placed two 2.6 centimeter high obstacles one behind the other on the path. That is quite a challenge, because a dung ball roller is less than a centimeter long. At these obstacles, the female no longer followed passively, as it turned out, but assisted by pushing or steering, and as a result, a pair cleared the double obstacle faster than a male working alone. Moreover, a male alone often gave up.

In a next series of experiments, the beetles were challenged with a wall of 3.9, 6.5 or 9.1 centimeters high. The higher the wall, the less likely a pair was to climb over it with the ball and the less likely it was to succeed if it tried. A male alone declined more often than a pair, but if he tried to clamber over the wall, he usually succeeded.

A couple could get over a high obstacle faster than a male alone, mainly because the female helped at the start. When the male pulled himself up along the wall and lifted the dung ball from the ground, she stabilized the ball with her hind legs and pushed it, in a headstand position. Then he worked his way up, while she hung on the ball. Despite that extra burden for the male, a pair climbed as quickly as a male alone. If he was in danger of falling, she would provide support. Once she got to the top, she became active and pushed the ball over the edge with her head. The beetles then fell down and continued their path.

Dung ball rollers manage to get their ball over difficult obstacles. Unlike the Greek mythical king Sisyphus, after whom the beetles are named. Because of his brutality towards the gods, he was punished by having to push a boulder up a slope in the underworld for eternity, while the boulder kept falling back. He could not do it alone and he did not have a partner to lend a hand.

Willy van Strien

Photo: Sisyphus schaefferi couple with dung ball, male at left side, female at right side. Daniel Ballmer (Wikimedia Commons, Creative Commons, CC BY-SA 4.0)

Watch the dung beetles’ behaviour on YouTube

Sources:
Tocco, C., M. Byrne, Y. Gagnon, E. Dirlik & M. Dacke, 2024. Spider dung beetles: coordinated cooperative transport without a predefined destination. Proceedings of the Royal Society B 291: 20232621. Doi: 10.1098/rspb.2023.2621
Dacke, M., E. Baird, B. el Jundi, E.J. Warrant & M. Byrne, 2021. How dung beetles steer straight. Annual Review of Entomology 66: 243-256. Doi: 10.1146/annurev-ento-042020-102149

Pharmacy on back

Matabele ant with a mouthful of termites

Groups of Matabele ants (Megaponera analis) hunt termites, which fight back fiercely. Consequently, foraging trips cause many casualties. An ant colony would perish if it were not for the fact that ‘slightly’ injured specimens, for instance ants that lost one or two legs, are picked up and carried back to the nest. Thanks to the care they receive there, most of them recover from their injuries; without help, they would be dead within 24 hours in all probability.

Erik Frank and colleagues previously discovered that workers lick and groom the wounds immediately after arrival in the nest. Now, it appears that they also treat the wounds medically. The Matabele ant lives in Africa south of Sahara; the research was done in Ivory Coast.

Video recordings in artificial nests in the lab show that workers groom victims’ wounds again after 10 to 12 hours, and then often apply a substance after cleaning that they take from glands on the back, the metapleural glands. They use their own glandular product or that of the wounded individual. They mainly treat ants with wounds that have become infected, for example with the deadly bacterium Pseudomonas aeruginosa.

The glands of the Matabele ant form a well-supplied pharmacy. They turn out to produce more than a hundred compounds, many of which have an antimicrobial or healing effect. Tests show that the antibiotic mix suppresses the growth of the bacteria. Most other ant species also have metapleural glands, but with a less extensive arsenal of substances.

How do nursing workers know whether a wound is infected or not? Probably because the composition of the outer layer that ants have – a waxy layer of hydrocarbons – changes during infection. Colony mates can smell that.

Conclusion: Matabele ant workers can effectively treat wounds of conspecifics with self-made antibiotics. This ability is unique among insects and other invertebrates.

Willy van Strien

Photo: Matabele ant worker with termites. ETF89 (Wikimedia Commons, Creative Commons CC BY-SA 4.0)

Former research on Matabele ant

Source:
Frank, E.T., L. Kesner, J. Liberti, Q. Helleu, A.C. LeBoeuf, A. Dascalu, D.B. Sponsler, F. Azuma, E.P. Economo, P. Waridel, P. Engel, T. Schmitt & L. Keller, 2023. Targeted treatment of injured nestmates with antimicrobial compounds in an ant society. Nature Communications 14: 8446. Doi: 10.1038/s41467-023-43885-w

Purple-crowned fairywren assists dear breeders

purple-crowned faiywren helps parent and potential partner

The number of territories available is limited for purple-crowned fairywren, a small passerine bird that lives in northern Australia in dense vegetation along rivers and creeks. The territories are linearly aligned, are kept all year round and are all occupied. Out of necessity, young birds often stay with their parents for a few years; most breeding pairs have a few male and female subordinates around them. Purple-crowned fairywrens, Malurus coronatus, eat insects; males have a beautiful purple crown during the breeding season.

Subordinates can assist the breeding pair during the busiest time, the two weeks when the young need to be provisioned. But not all of them offer help, and not all helpers work equally hard. Group members that don’t help are still allowed to stay in the group. Niki Teunissen and colleagues investigated under which circumstances group members do or do not help well. They show that a purple-crowned fairywren subordinate ‘knows’ precisely when it pays to be helpful.

The researchers provided birds with colour rings to make them individually recognizable and of each bird, they knew its parents and its brothers and sisters. They observed the behaviour of fifty groups during three breeding seasons.

If young in the nest have the same parents as a subordinate, or share one parent with it, that subordinate will help feed them. And that is worth the effort. Because with help, more young fledge per clutch on average. A helper shares in this greater success, because those young are full siblings or half-siblings. But in the few years that children stick around, both parents may have died or disappeared and been replaced. And sometimes young birds do not join their parents, but another couple. In such cases, the young are unrelated and a subordinate will not help raise them.

Kinship with the young does not fully explain the willingness to help, though, because, on average, group members work harder for a clutch of half-brothers and half-sisters than for a clutch of full brothers and sisters. That seems enigmatic, but something else is going on. Whether a subordinate will support a breeding pair and how hard it will work, also depends on the value that the pair itself has.

When both the breeding male and female are not its parents, it is not going to help feed the young, as we already saw. If both are its parents, it will help; the young are then full siblings. Thanks to this help, the parents reduce their workload. Their chance of survival increases, and so does the chance that a new clutch of brothers and sisters will be produced. This is also a win for the helper.

Things get interesting, the researchers discovered, when one parent is gone and the other parent has a new partner. How hard a resident purple-crowned fairywren will work now depends on which parent is left: the same-sex parent or the other one.

A female purple-crowned fairywren living with her mother and her new partner works much harder than a subordinate in a group with both parents. That is because that new male partner is interesting. If her mother dies, the helper may inherit her place and her partner, become the owner of the territory and produce the next clutch. That’s the main prize!

With a father and a new partner, she has less to gain. That new female partner is of no use to her, in fact: she is a rival if a new male ever comes into play. So, she works less hard.

Likewise, a male fairywren puts in most effort in helping when living with a father with a new partner.

And therefore, a subordinate purple-crowned fairywren works hardest when the breeding pair consists of a parent and a potential mate – which is very sophisticated. Such couple has great value to him or her. That is why he or she often helps provisioning a nest with half-siblings more intensively than a nest with full siblings.

In line with this, the researchers had previously shown that a young purple-crowned fairywren is less willing to join a group with a same-sex stepparent. Subordinates affiliate with parents and a potential mate. Also, when they help defend the nest against predators, it is to protect (half)siblings as well as parents and a potential mate.

Willy van Strien

Photo: Female (left) and male purple-crowned fairywren. P. Barden (Wikimedia Commons, Creative Commons CC BY 4.0)

Sources:
Teunissen, N., M. Fan, M.J. Roast, N. Hidalgo Aranzamendi, S.A. Kingma & A. Peters, 2023. Best of both worlds? Helpers in a cooperative fairy-wren assist most to breeding pairs that comprise a potential mate and a relative. Royal Society Open Science 10: 231342. Doi: 10.1098/rsos.231342
Teunissen, N., S.A. Kingma, M. Fan, M.J. Roast & A. Peters, 2021. Context-dependent social benefits drive cooperative predator defense in a bird. Current Biology 31: 4120-4126. Doi: 10.1016/j.cub.2021.06.070
Teunissen, N., S.A. Kingma, M.L. Hall, N. Hidalgo Aranzamendi, J. Komdeur & A. Peters, 2018. More than kin: subordinates foster strong bonds with relatives and potential mates in a social bird. Behavioral Ecology 29: 1316-1324. Doi: 10.1093/beheco/ary120
Kingma, S.A., M.L. Hall, E. Arriero & A. Peters, 2010. Multiple benefits of cooperative breeding in purple-crowned fairy-wrens: a consequence of fidelity? Journal of Animal Ecology 79: 757-768. Doi: 10.1111/j.1365-2656.2010.01697.x

Suicide on command

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

Promotion for buff-tailed bumblebee worker

If the queen is lost, a worker can take over

When the queen is lost, a buff-tailed bumblebee worker can take over

Normally, buff-tailed bumblebee workers do not mate. But if the queen disappeared, they may mate, Mingsheng Zhuang and colleagues show, enabling the colony to survive.

A bee queen mates and lays eggs; fertilized eggs develop into females, unfertilized eggs into males. Her workers, also females, refrain from reproduction; they defend the nest, care for the brood and forage for food. Thanks to this strict division of labour, a colony runs well. If workers also would produce eggs, too little work would be done. Because the offspring of the queen are related to each other, workers have indirect reproductive success. They do not have a spermatheca, the vesicle in which females store sperm after mating, and are unable to mate. Once a worker, always a worker.

At least, this is how it is in honeybees.

But it does not apply to all bee species that live in colonies with a division of labour between queen and workers, so-called ‘eusocial’ species. In bumblebees (which belong to the bees), workers do have a spermatheca.

It was a mystery why. Now, Mingsheng Zhuang and colleagues argue that bumblebee workers sometimes are promoted to queen.

Artificial insemination

Zhuang shows that workers of several bumblebee species have a spermatheca that is functional. When he artificially inseminated workers, they responded in the same way as queens. They laid fertilized eggs from which daughters emerged and founded a colony. He thinks that workers of all bumblebee species still have a functional spermatheca, even though bumblebees have existed as a eusocial group for tens of millions of years.

The logical next question is whether bumblebee workers can actually mate and function as queens. And under what circumstances they will do.

The researchers conducted much of their research on the buff-tailed bumblebee, Bombus terrestris. This species, which occurs in Europe, North Africa, and parts of Asia, has colonies that exist for one year. In the spring, each queen that has mated and hibernated starts a colony on her own. She makes a nest in the ground, lays eggs and takes care of the larvae that hatch. These larvae develop into workers. Once they are present, the queen is dedicated to laying eggs. The colony grows to a size of hundreds of workers.

At the end of the season, the queen lays eggs from which males develop, and young queens appear. Workers also will lay eggs then, which are unfertilized and produce males. Young queens leave, mate and search a place to hibernate. Males and workers die.

Replacement

Buff-tailed bumblebee workers normally do not mate. But they can, as experiments of Zhuang show, if they have been separated from the queen and egg-laying workers for a while. In this regard, they differ from young queens, which do not need such a period of isolation. And if a worker has been in the company of nest mates for more than 24 hours before isolation, a switch is not possible anymore. So, opportunities for promotion are limited. Moreover, the chance of workers surviving a mating appears to be small.

But it may be enough to be able to provide a replacement and rescue the colony if a queen dies prematurely, Zhuang and colleagues think; that chance is probably quite high. In that case, workers will lay eggs that develop into early males and if one of the workers takes over the role of queen, mating and producing daughters, the colony can finish the season. According to them, this explains why workers have retained a functional spermatheca. It is difficult to determine whether such replacement often occurs in the wild, they write. It would require locating and digging out colonies and conducting DNA research.

Smaller

Why doesn’t a worker leave the natal colony and start her own? She would have to leave soon after eclosion, meet a male and survive the mating. But workers are much smaller than queens and produce fewer eggs. Being part of a large colony as a worker will yield greater reproductive success than heading a small colony as a queen.

Willy van Strien

Photo: Buff-tailed bumble bee queen on small-leaved lime. Ivar Leidus (Wikimedia Commons, Creative commons CC BY-SA 4.0)

Source:
Zhuang. M., T.J. Colgan, Y. Guo, Z. Zhang, F. Liu, Z. Xia, X. Dai, Z. Zhan, Y. Li, L. Wang, J. Xu, Y. Guo, Y. Qu, J. Yao, H. Yang, F. Yang, X. Li, J. Guo, M.J.F. Brown & J. Li, 2023. Unexpected worker mating and colony founding in a superorganism. Nature Communications 14: 5499. Doi: 10.1038/s41467-023-41198-6

Only when the weather is cool

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

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