Unopened flower

Moth larva enforces self-pollination in Canada Frostweed

Canada Frostweed may be enforced to self-pollination by a moth larva

The larva of the moth Mompha capella inhabits a flower bud of Canada Frostweed and prevents it from opening, as Neil Kirk Hillier and fellow researchers show. Pollinators cannot visit the flower, which has to pollinate itself instead.

Canada Frostweed (Crocanthemum canadense), a perennial plant of Northern America, is attractive to the moth Mompha capella, which lays its eggs on it. Then something unusual happens: the plant loses control over its reproduction.

The plant produces yellow flowers that normally open just after sunrise, revealing the female pistil and male stamens. Bees and flies visit the flowers, transferring the pollen from one to the next, so that the flowers are cross-pollinated. Multiple stamens lay against the five yellow petals, retracted from around the pistil to prevent self-pollination. Within a few hours, a flower’s own pollen has disappeared and the pistil is covered with pollen from other flowers. The petals fall off, the green sepals close over the pistil and protect the developing fruit with seeds within.

But when a moth has left its eggs on the plant, the larvae that hatch from these eggs crawl into a flower bud, one larva per bud. And then things are very different, Neil Kirk Hillier and colleagues discovered.

Cap

The larvae start to eat. And they don’t do it randomly, but first feed on the bases of the still folded petals. The severed petals no longer grow and don’t unfold when the flower should open, but remain folded like a cap over stamens, pistil and developing fruit, keeping the flower closed. Pollinators cannot enter. Because the stamens are compacted around the top of the pistil, the pollen is in contact with the pistil and seeds develop through self-pollination. Almost all of them will be consumed by the larva in the end.

Frostweed duped

As a consequence, the Canada Frostweed plant produces less offspring. A yellow flower produces on average about forty seeds, and a larva saves only one or two of them. Reproduction, however, is not in immediate danger. This is because the plant not only produces a small number of yellow flowers that open, unless caterpillar disturbs the process, but also a large number of flowers without yellow petals and only four or five stamens, which appear later in the year. These flowers never open and produce seeds through self-pollination. While they make less seeds than yellow, open flowers (only six or seven seeds per flower), there are much more of them. So seeds are produced anyway.

But seeds of open flowers that develop after cross-pollination are necessary for the exchange of hereditary material. In plant populations with a high infestation rate, such exchange is limited, and genetic variation is low.

Larva safer?

The researchers don’t mention what benefit a larva gains by intervening in the flowering process. If the flower opened and had been pollinated normally, seeds to be consumed would have appeared as well. Perhaps in a closed flower, the larva is safer from predators and parasites.

Willy van Strien

Photo: Homer D. House, 1918 (Wikimedia Commons)

Source:
Hillier, N.K., E. Evans & R.C. Evans, 2018. Novel insect florivory strategy initiates autogamy in unopened allogamous flowers. Scientific Reports 8: 17077. Doi:10.1038/s41598-018-35191-z

Role pattern erased

Twisted-wing parasites change the behaviour of host wasps

The paper wasp Polistes dominula is host to a manipulating parasite, Xenos vesparum

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: ©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

Gruesome boost

Damaged cicadas spread fungal spores via sexual behaviour

Magicicada species are manipulated by the fungus Massospora

Massospora fungi produce substances that we know as recreational drugs, Greg Boyce and colleagues write. By doing so, they manipulate the behaviour of cicadas in which they proliferate. The insects face a horrible fate.

The fungus Massospora cicadina infects periodical cicadas of the genus Magicicada and manipulates the behaviour of infested insects in such a way that they will transmit the fungal spores to conspecifics. Horribly enough, they do so by sexual activities, while their rear part has already been largely destroyed and turned into a fungal mass. Greg Boyce and colleagues try to find out how the fungus exerts its dismal influence.

Magicicada species, which live in the east of North America, are almost never to be seen. They spend most of their life underground as nymphs, the immature form. Only once in many years – some species take thirteen years, other species take seventeen years – mature nymphs emerge from the soil, synchronously and massively per species and per area. They moult into mature cicadas that live only for four to six weeks. In this period, they mate and the females lay their eggs on tree branches. Young nymphs fall down and disappear in the soil.

This unusual life cycle makes it very difficult for natural enemies such as birds to specialize on adult cicadas, because they would not be able to find prey for many years while occasionally, once in thirteen or seventeen years, there is an overwhelming amount.

But the fungus Massospora cicadina can deal with the life cycle of these cicadas.

Copulation attempts

Fungal spores rest in the soil until nymphs emerge and then infect them. After moult, the fungus proliferates in the abdomen of adult insects. Eventually, their rear part, genitals included, falls off and a fungal spore mass becomes visible.

The heavily damaged cicadas try to mate, even more vigorously than normal. Of course, this is useless to them, but the fungus benefits: during the copulation attempts, the unfortunate cicadas transmit spores to conspecifics.

In these insects, the fungus forms a second infection stage. Because now time runs out for the adult cicadas, a third infection is not feasible. Therefore, instead of infective spores, the fungus produces resting spores, which fall down and wait in the soil until the next generation of cicadas appears.

Bisexual males

Earlier this year, John Cooley and colleagues described deviant behaviour in males with a first stage infection. Normally, males sing in chorus to lure females. When a female shows interest in a male, she makes a flicking wing movement that is tuned to his song. He then utters more complex song, she answers with a tightly timed wing-flick, and a ‘duet’ is created while the two approach each other.

First stage infected males try to acquire a female mate in the normal way. But they also respond to the song of other males with female-like wing-flicks. As a result, not only females, but also males are attracted – and become infected. The fungal infection spreads extra fast.

It is striking that only males with a first stage infection assume a female role besides a male role. Males with a second stage infection, which does not produce infective spores, don’t exhibit wing-flicks.

Stimulating drug

Now, Greg Boyce shows how the fungus manages to affect the behaviour of the cicadas. Among the substances that it produces in the cicadas’ abdomen is cathinone. This is known as the active substance in khat, which is released when chewing leaves of the Khat plant, Catha edulis. It is surprising that a plant and a fungus share this substance. Cathinone is closely related to amphetamine, or speed, a stimulating drug, and just like the drug, it interferes with the communication between nerve cells. Apparently, this results in abnormal behaviour in male cicadas.

In a first stage infection, in which the cicadas transmit the fungus spores to conspecifics, the fungus produces more of this stimulating substance than in a second stage infection, which shows how accurately it manipulates its host.

Another Massospora fungal species, which infects cicadas with an annual cycle (Platypedia species), also manipulates the sexual behaviour of its victims, Boyce and colleagues discovered. It produces psilocybin, a hallucinogenic substance known from certain mushrooms, most importantly Psilocybe species. Again a remarkable finding, as the fungus is not closely related to these mushroom species.

Willy van Strien

Photo: Magicicada septendecim. Judy Gallagher( Wikimedia Commons, Creative Commons CC BY 2.0)

Sources:
Boyce, G.R., E. Gluck-Thaler, J.C. Slot, J.E. Stajich, W.J. Davis, T.Y. James, J.R. Cooley, D.G. Panaccione, J. Eilenberg, H.H. De Fine Licht, A.M. Macias, M.C. Berger, K.L. Wickert, C.M. Stauder, E.J. Spahr, M.D. Maust, A.M. Metheny, C. Simon, G. Kritsky, K.T. Hodge, R.A. Humber, T. Gullion, D.P.G. Short, T. Kijimoto, D. Mozgai, N. Arguedas & M.T. Kasson, 2018. Discovery of psychoactive plant and mushroom alkaloids in ancient fungal cicada pathogens. BioRxiv preprint, July 24. Doi: 10.1101/375105
Cooley, J.R., D.C. Marshall & K.B.R. Hill, 2018. A specialized fungal parasite (Massospora cicadina) hijacks the sexual signals of periodical cicadas (Hemiptera: Cicadidae: Magicicada). Scientific Reports 8: 1432. Doi: 10.1038/s41598-018-19813-0
Cooley, J.R. & D.C. Marshall, 2001. Sexual signaling in periodical cicadas, Magicicada spp. (Hemiptera: Cicadidae). Behaviour 138, 827-855. Doi: 10.1163/156853901753172674