Why Evolution is True is a blog written by Jerry Coyne, centered on evolution and biology but also dealing with diverse topics like politics, culture, and cats.
Tony Eales from Australia has sent us some insects and spiders fatally infected with parasitic fungus. TRIGGER WARNING: ARTHROPOD DEATH! His captions are indented, and you can enlarge the photos by clicking on them.
With the TV show The Last of Us and its fungi infected zombie antagonists in the zeitgeist, I thought I’d send through some pics of entomopathogenic fungi that I haven’t sent before.
This first one is either icing sugar fungus or a close relative, Beauveria sp. infecting a native wood cockroach (Family Ectobiidae) of some sort. It was hard to tell if the picture was in focus or not with the diffuse fuzzy nature of the fungus
Next might be a fungus in the family Entomophthoraceae. This family generally infect flies and other dipterans but there is a genus that specialises in cicadas, Massospora spp. Perhaps this is related? The host cicada is or Frog Cicada.
Both the previous fungi I found in the tropical rainforests of North Queensland. The rest of these are from the subtropical areas around Brisbane, southeast Queensland.
Here we have the more typical form and host of Entomorpthoraceae, one of the fly-death fungus species complex. They are easily recognised by the way the light-coloured fungi bursts from between the darker abdominal tergites forming a striped look to the dead fly.
The rest of the fungi are in the family Cordycipitaceae as was the Icing Sugar Fungi up top.
Since I spend a lot of time looking for hidden and well camouflaged spiders, I come across a lot of Gibellula ssp. This group of fungi really like spiders and I am presuming that the hosts in all of these following five pictures are small spiders of one sort or another (although with some it’s very hard to tell).
The only one that I can ID to species is the last one. This unfortunate is a male Green Jumping Spider, Mopsus mormon, the largest jumping spider in Australia and common garden resident in subtropical areas.
Next is what I suspect is Hirsutella sp. I really can’t tell much about the host but I have seen Hirsutella on planthoppers before and the location under a leaf would be consistent with this group.
And lastly Ophiocordyceps dipterigena, another species that targets flies. I often found it on robber flies perched out on the end of twig in drier forests in SE Queensland.
Today’s bit of enlightenment comes from Athayde Tonhasca Júnior, and is on a subject that makes some people squeamish. But read on!
‘Thick-headed undertakers in the night of the living dead’
If you watched Alien, you may have jumped out of your seat when the baby monster burst from the astronaut’s chest. But an entomologist may have nodded knowingly: ‘Ah, a human parasitoid!’ Indeed, the screenwriters acknowledged entomological inspirations for coming up with the alien’s life cycle.
Here on Earth, a parasitoid is an insect whose larva develops inside the body of a host (usually another insect), eventually killing it. This type of life history lies between a predator’s and a parasite’s: a predator such as a dragonfly takes several prey and kills them outright, while parasites such as lice, fleas and ticks live off hosts without killing them.
Wasps account for most parasitoid species, but quite a few of them are flies. These include the 800 or so species of thick-headed flies (family Conopidae). A look at one of them explains their common name, although some species look more like wasps or bees than flies. They are also known as bee-grabbers or conopids.
Thick-headed flies hang around flowers looking for a sip of nectar. But a female may have other ideas: she may be waiting for an opportunity to lay her eggs, which is bad news for a bee or wasp.
It goes like this: an unsuspecting bumble bee worker approaches a flower. A female conopid closes in and grabs the bee in mid-air. Still afloat, she pries open the bumble bee’s abdominal segments with her theca, which is a pad-like, hardened structure at the end of her abdomen. Sometimes attacker and victim fall to the ground, but the outcome is the same; the female fly lays a single egg inside the bumble bee and lets it go.
The drama is over within seconds, and both insects fly away. The fly will stalk another quarry. But the bumble bee is done for.
The egg hatches and the conopid larva develops inside the bumble bee, consuming her innards. But the larva does not penetrate the host’s thorax, thus leaving her flight muscles intact. The bee carries on with her life, feeding and taking nectar back to her nest, although less and less efficiently as the parasitoid grows. Within 10 to 12 days her abdomen is completely taken up by the larva, which has nothing more to eat. The bee dies and falls to the ground (if you find a dead bumble bee with a swollen abdomen, conopid parasitism could be the causa mortis). The larva pupates and overwinters inside the bee’s body, and the adult emerges in the following year.
Some conopids increase the chances of their pupae making it through the winter with a trick that may seem macabre to human eyes: they induce their bumblebee hosts to dig their own graves. In North America, bumblebees parasitized by the conopid Physocephala tibialis bury themselves in the ground just before popping the clogs. This grave-digging behaviour does not make a difference for the bee, but the parasitoid pupa is sheltered from cold and dehydration during winter months, and less exposed to pathogens and its own parasites. Hibernation in the soil also promotes larger and healthier adult flies.
But bees don’t take it lying down. When parasitism pressure becomes too high, some species reproduce later in the year to avoid peaks of conopid populations. And some bumblebees – like many other insects – secrete melanin, which encapsulates and suffocates internal parasites. It is estimated that melanisation kills up to 30% of conopid larvae.
After a parasitized bumblebee has dug its burial pit somewhere in America, a cold, drizzly night falls over the land. All is quiet. Until in an apiary nearby, one of the resident honey bees (Apis mellifera) does something odd: she emerges from the hive and flies towards a streetlight glowing faintly in the distance. A few of her sisters follow suit, although some of them fall to the ground and begin walking around in circles, apparently confused. None of these night wanderers will ever return to the hive; soon they will all be dead. They have been victims of a parasitoid ominously named the zombie fly (Apocephalus borealis).
This fly belongs to one of the largest insect groups, the family Phoridae. They comprise about 4,000 described species, but specialists believe this number represents a fraction of the total. Phorids look like fruit flies with arched backs, and when spooked they run away before taking flight. Such behaviours explain their common names: hump-backed flies or scuttle flies. They are everywhere, and have a variety of feeding habits such as saprophagy (they eat decaying organic matter), predation, and herbivory. One species is a serious pest of cultivated mushrooms.
Two groups of Phorid flies, the genera Pseudacteon and Apocephalus, are found mostly in South America and are charmingly known as ant-decapitating flies. A typical species approaches an ant from behind and uses its powerful, hooked ovipositor to inject an egg in the victim’s head or thorax.
The resulting larva moves to the ant’s head, where it feeds on hemolymph (‘blood’) and tissues. Eventually, the larva consumes all the head’s contents, causing the ant to wander around erratically. In two to four weeks, the larva is ready to pupate. It releases enzymes that dissolve the tissues attaching the ant’s head to its body. The head falls off, and the fly pupates inside it before emerging as an adult. These flies are efficient ant killers, and therefore are promising biological control agents against invasive species such as fire ants (Solenopsis spp.).
The zombie fly does not decapitate honey bees, but much of its life history is similar to those of its tropical relatives. It lays its eggs in the abdomen of the bee. The larvae feed on hemolymph and flight muscles, and when they are done, they leave the host to pupate outside. Up to 13 larvae have been observed coming out of a dead honey bee.
We don’t know why a parasitized honey bee abandons her nest, especially at night, to wander on a suicidal excursion. Her neurological wiring may have been highjacked by the fly, inducing the bee to seek a safer place for the development of the parasitoid’s eggs and larvae. The bee may have been forced out by her healthy sisters; or she left the colony on her own, acting on an altruistic instinct to avoid an epidemic.
The zombie fly is native to North America, where it has long been known to parasitize bumble bees and wasps. Then in 2009, there was an alarming discovery: the fly was also attacking honey bees in parts of the country. And there was more bad news to come. The zombie fly harbours the fungus Nosema ceranae and the Deformed Wing Virus, which are serious threats to honey bees. Researchers don’t know yet whether the zombie fly plays a role in the transmission of those pathogens to bees, but the possibility is worrying.
Conopids and zombie flies are some of the many parasites and parasitoids capable of changing hosts’ behaviour for their own benefit. Some wasps turn ladybirds into paralysed living shields over their eggs, and some fungi make ants climb up plants so they can release spores into the air. Perhaps the most notorious case is the effect of toxoplasmosis cells on rats and mice. Infected rodents become attracted to cat’s urine and are less likely to hide. This altered behaviour is a death wish: they became easy prey for cats, in which toxoplasmosis cells complete their development. Carl Zimmer discussed many other examples in his excellent Parasite Rex; you can read about some of them here.
Parasitism seems gruesome and cruel. Even Darwin was dismayed by it, as he expressed in one of his letters: ‘I cannot persuade myself that a beneficent & omnipotent God would have designedly created the Ichneumonidæ [ a group of parasitic wasps] with the express intention of their feeding within the living bodies of caterpillars.’* But such anthropomorphism is misguided and biased. Parasitoids, predators and parasites are regulators of the natural world: about 10% of all known insect species are parasitoids, although specialists believe this figure is a huge underestimation. They prevent excessive population growth, including of agricultural pests and disease vectors. Parasitism helps shape biodiversity and ecosystems, so it is not intrinsically bad or good. It is a characteristic of life on our planet.
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* This famous quotation inspired a team of ichneumonid specialists to propose in 2019 ‘Darwin wasps’ as a vernacular name for this group of insects, so that they may become better known and appreciated.
Today we have a special contribution by Athayde Tonhasca Júnior. The photos are not his, but he’s writteen an illustrated mini-essay on a case of parasitism. Athayde’s words are indented, and you can enlarge the photos by clicking on them. You don’t often see life cycles as complicated as this one!
If you are getting low on wildlife contributions, your readers may enjoy -(or be horrified by, depending on one’s take) an introduction to stylopids.
Stylopized, emasculated and zombified: the risks of visiting a flower
‘Bizarre’ and ‘weird’ are overused adjectives for describing many characters and events of the natural world. Life is way too complex and varied to conform to familiar patterns, so the out-of-the ordinary is all around us, even though we not always see it. But when the discussion turns to stylopids, it’s difficult to avoid talking about the bizarre and the weird.
Stylopids (or stylops) are small, seldom seen and poorly known insects with about 700 described species, 10 to 16 of them in Britain. The true figures are likely to be much higher. They are parasites of other insects such as bees, wasps, plant hoppers and leaf hoppers. From a distance, male stylopids can be mistaken for flies, but their ruffled wings give them away and explain the name of this group of insects: the order Strepsiptera, from the Greek strephein (to twist) and pteron (wing). Twisted-wing insects is another common name for them.
Males have branched antennae and their eyes are berry-like structures comprising dozens of image-forming eyelets. This unusual array inspired the development of new cameras of reduced size and sharp images, which are handy for smartphones. Males cannot feed because their mouthparts are not developed. But never mind going hungry; they don’t live for more than a few hours. Their only objective in life is to use their fancy eyes to find a female and mate.
Females look nothing like the males. In fact, they don’t look like your ordinary insect at all because they don’t have wings, antennae, legs, mouthparts or eyes: they are neotenic, i.e., they retain their larval features. An adult female does not need a fully formed body since she never leaves her host: she will develop and die semi-buried in another insect. ‘Semi-buried’ because the tip of her cephalothorax (the head and the thorax fused together) protrudes from the host’s abdomen.
Through this exposed area, the female releases a pheromone to attract males. Once suitors finds her, they face an anatomical challenge. Only parts of her head/thorax are exposed, which doesn’t bode well for conventional insect romance. But this setback is nothing compared to the facts that she doesn’t have genitalia, and her eggs float in the haemolymph (‘blood’). So a male has only one course of action: the disturbingly sounding traumatic or hypodermic insemination. He pierces the female’s cuticle with his penis and injects his sperm into her haemolymph. Watch it at this link.
The deed done, males soon die. The fertilised eggs hatch inside the female, giving birth to thousands of tiny planidia (singular planidium, from the Greek planis, meaning ‘wanderer’). These are a type of larva that don’t look at all like larvae. They have well developed legs, are quite nimble, and they’re phoretic, that is, they use another organism to be transported to a new location. The planidia feed on mum’s innards and eventually crawl out of her body to disperse and start looking for a host of their own.
A wandering planidium climbs a flower to wait for an unsuspecting visitor. When a bee or wasp lands, the planidium somehow hitchhikes a ride to their nest. We are not sure how it does this: it could hide in the pollen, or possibly be swallowed with the nectar sucked up by the flower visitor, then released when the host regurgitates nectar inside the nest. Chances are it will end up in the wrong nest, so most planidia are done for. But the staggering fecundity of female stylopids compensates bad odds: they can dish out 750,000 planidia, so a few are likely to find a suitable host.
Once inside the right nest, the planidium burrows into a host’s egg or larva and transforms into a traditional legless, grub-like larva. It is followed by other larval stages, pupation, and finally adulthood – by then the host has also become an adult. If it’s a male stylopid, it squeezes out of the host and flies away, usually leaving a big gap behind and killing the host. If it’s a female, it will park itself in the host’s abdomen.
The story above is a peep at stylopids’ life histories, as there is considerable variation depending on the species and type of host. And if all this sounds outlandish, there is more to come:
Stylopization (parasitism by stylopids) causes all sorts of physical and behavioural eccentricities in the host, all for the parasite’s advantage. Host infertility is one example. Reproduction involves mating, nest building, nest provision, etc., all of which are risky and energy-consuming, and therefore not beneficial for a parasite. Stylopids solve this problem by disabling the host’s reproductive organs, functionally castrating them. Some stylopized bees have reduced scopae (pollen-carrying structures) and seldom if ever carry pollen: there’s no point, as they don’t have a brood to provide for. Contrary to what happens to most parasitized insects, stylopization often lengthens host development; they live longer so that stylopids have more time to mature. Some stylopized bees are led to stand still on a grass or flower stems with their head downwards. Such a zombie state greatly facilitates stylopids’ mating business.
In Britain, furrow bees (genera Halictus and Lasioglossum), yellow-face bees (genus Hylaeus) and especially mining bees (genus Andrena) are victims of stylopids, but we have little information about their interactions and no idea about consequences of parasitism.
Stylopids are odd and enigmatic, but they are also one of the most complex and intriguing groups of animals. They are evolutionary marvels that have puzzled and awed generations of entomologists and naturalists, and more surprises will be revealed from future research. It seems quite fitting, then, for the august Royal Entomological Society to have adopted a stylopid (Stylops kirbii) as a representative of the organisation:
I am running dangerously low on photos, and worry that I will have to cancel this feature or make it more sporadic. If you have good wildlife (or “street”) photos, please send them in pronto. If you’re an American, you have a long weekend coming up to peruse your photos.
All photographers’ words and captions are indented, and you can enlarge the photos by clicking on them.
We have a potpourri today, the first coming from reader Jonathan Storm.
I found this dead grasshopper on an eastern hemlock in the Blue Ridge Mountains of South Carolina. It was killed by an entomopathogenic fungus last summer or fall. These fungi are parasites that infect and eventually kill their insect host. Last summer, a fungal spore landed on this grasshopper and worked its way into the body cavity. The fungus then grew and spread until it killed the grasshopper. Several fruiting bodies of the fungus later grew out of the grasshopper and released their spores into the breeze. Some of these spores will then infect a new insect host and the cycle continues.
A gorgeous Cyclops moth (Antheraea polyphemus) from reader Smith Powell, photographed by Jennifer Lawson:
My granddaughter, Jennifer Lawson, photographed this moth on 02 May 2021 in the family yard in Arlington, Texas. I think this is the prettiest photograph that I have seen of Antheraea polyphemus.
As I’m not a biologist, I had no idea what it was, but I was quickly able to identify it as the Cyclops moth. Indeed, several websites so identify it and note that it is named for the race of one-eyed Cyclops famously described in the Odyssey. The sites even say that Cyclops means one-eyed.
But, it doesn’t! Besides, this moth has two eyespots. Cyclops means “round eye”. And this photograph shows the eyespots as very round or spherical.
Jennifer’s father, Clint, told me, “ We used to tell our baseball umpires ‘if you had another eye you’d be a cyclops ‘“.
And a pair of Great Tits from reader Pyers:
A Great Tit (Parus major) saying hello from the nest box in my garden:
And have a female Great Tit. the even more cute partner of the one I sent you the other day 🙂
I am running worryingly low on readers’ photos, so PLEASE send in your good ones. I don’t want to have to cancel this feature or put it up sporadically. Thanks!
We have a potpourri of photos and movies today. Readers’ captions are indented, and you can enlarge the photos by clicking on them.
The first two photos are by Andrea Kenner.
Here’s a photo of my first sighting of a Brood X cicada. The baby is sitting on the sidewalk in Hyattsville, Maryland. I’m not sure which species he is (there are three). Here’s a link to the Wikipedia page.
I took this photo in my front yard in Prince George’s County, MD, and posted it on Facebook. The tree is an Eastern Redbud (Cercis canadensis). An entomologist in my neighborhood identified the bee as a Hairy Footed Flower Bee (Anthophora villosula), a recently introduced species in the Mid-Atlantic region.
From Linda Mercer:
It is hard to see the tiny fawn hiding behind my air conditioner.
A duck video from Brian Tarr:
I’ve been an avid lurker on your excellent website for several years, and have finally plucked up the courage to share a bit of wildlife with you. This is a sord of mallards which I filmed this last winter in Łuków, Poland, by the Southern Krzna River in the central park. I thought it a bit unusual to see so many, because I figured they would have flown south by then. As you can see, they are quite accustomed to humans, as people often come with their children to toss them bread (not the ideal diet, as I learned from you).
Please feel free to share this with your readers, if you so choose. I would love to get some feedback about migratory patterns. (Possible aberration due to climate change?)
And a parasitized grasshopper from Jonathan Storm:
I found this dead grasshopper on an eastern hemlock in the Blue Ridge Mountains of South Carolina. It was killed by an entomopathogenic fungus last summer or fall. These fungi are parasites that infect and eventually kill their insect host. Last summer, a fungal spore landed on this grasshopper and worked its way into the body cavity. The fungus then grew and spread until it killed the grasshopper. Several fruiting bodies of the fungus later grew out of the grasshopper and released their spores into the breeze. Some of these spores will then infect a new insect host and the cycle continues.
And a video from Jonathan:
This female Ruby-throated Hummingbird [Archilochus colubris] was collecting spider silk from a window on my house in South Carolina. The sticky and stretchy nature of the silk help hold the nest together and anchor it on top of a tree branch. Ruby-throated Hummingbirds often construct their nest from dandelion seeds, moss, and lichens and place it high up in a hardwood tree.
Tony Eales from Queensland weighs in with photos documenting a nice story of parasitism and mimicry, with the mimicry being an orchid that deceives a male wasp into trying to copulate with it. (The gain is pollination for the flower; the wasp gets nothing but frustration.)
Tony’s descriptions are indented; click on the photos to enlarge them.
I came across something quite special on the weekend. It’s a terrestrial orchid Arthrochilus prolixus, AKA Wispy Elbow Orchid.
This orchid by sight and smell imitates a wingless female Thynnid wasp. Female Thynnids often sit at the top of a blade of grass waiting for a male to find them. It is this behaviour the orchid takes advantage of.
JAC: Note how the orchid above imitates a waiting female. The male mates with the orchid, getting pollen on its back, and then, because wasps aren’t that smart, eventually tries to mate with a different orchid, whereupon the pollen from the first orchid detaches and pollinates the second one. (Note the stamens in the orchid at lower right above.) This is known as pollination by “pseudocopulation.”
Thynnid males pick up females and carry them around while mating for many hours.
Thynnids are parasitoids of scarab beetle larvae. Scarabs live under ground or within litter for a year or more, feeding and growing. As larvae they are often known as Curl Grubs (and I realise I don’t have any photos of curl grubs which is strange, only adults). [JAC: see a photo here.]
The females deposit a single egg on any scarab larvae they find which grows and eats the larvae until emerging as an adult wasp and digging out.
Here’s a photo of a male I observed busily pulling back leaves off the ground as a newly emerged female was making her way out.
There are around 2000 species of Thynnid in Australia of which only about a quarter have been described and named. As far as I can tell no-one yet knows the species that pollinates the orchid that I found.
And here is a paper describing how a different species of elbow orchid tricks the wasps into getting a wad of pollen attached to the right spot on their back with great pictures.
When I first read the publicity about this recent (2017) paper in Proc. Nat. Acad. Sci., I thought that the authors had come up with a new solution to how the fungus Ophiocoryceps unilateralis, a parasite on carpenter ants, turns the ant into a zombie, behaving in a way that facilitates the dispersal of the fungus.
People are fascinated with this system because of the “zombie” connection, and because of the fact that a fungus (considered a “lower” species) can control the behavior of the ant. In this this case the fungus somehow causes the infected ant to climb onto vegetation, bite into it hard, and then die with its body extending out, allowing dispersal of the fungal spores into the air from a stalk that grows out of the ant’s corpse. The spores then disperse, and can fall on another ant so that the fungus begins it life cycle anew. Here’s the life cycle from MicrobeWiki:
And a photo of a dead and with the fungus sprouting from its body. Note how the ant has bitten into the vegetation to secure itself: a true death grip!
And here’s a Planet Earth video, with Attenborough narrating, showing the “attack of the killer fungus” Cordyceps (a different species that kills the same way) on bullet ants (a different species). But the principle is the same (though not necessarily the mechanism).
There are other examples of microbes or fungi controlling the behavior of their host in such a way to facilitate their own spread at the expense of the host’s life. A recently famous one involves the discovery that the protozoan parasite Toxoplasma gondiiappears to change the behavior of rodents—its intermediate host—making them lose their fear of cats. The rodents are then devoured more easily by cats, who then shed the eggs in their feces, infecting more rodents who come into contact with the feces. Here’s that life cycle (it has several life stages) from Wikipedia:
Parasites manipulating the behavior of their hosts to facilitate the spread—and, of course, the spread of the genes producing that host-altering behavior—is what Richard Dawkins calls an “extended phenotype”, with the new behavior being considered a trait of the parasite that produced it. However the parasites do this, it’s a marvel of evolution—a sophisticated “behavior” of simple organisms that arose via natural selection.
Up till when this paper was published, it’s always been thought that in the case of ants and “zombie-producing” fungi, the fungus invaded the host’s brain, changing its behavior in an adaptive way for the fungus (note Attenborough’s “explanation” in the video). Now, however, the 2017 paper by Maridel Fredericksen et al. shows that the fungus invades not the brain, but muscles in every part of the body (click on screenshot below, the pdf is here, and the reference and link at the bottom). In fact, most of us missed that paper, and continued to say in the last three years that the fungus turns the ant into a zombie by invading the ant’s brain.
That excited me at first, because I thought that the fungus was somehow manipulating the actual movement of the ant’s muscles, including that crucial clamping of the mandibles on the plant. But that doesn’t seem to be the case. The invasion of muscles may provide nutrients for the parasite, but is not yet seen as a way to control the ant’s behavior. What’s new, then, is that while we still don’t know how the “zombie” behavior arises, we know it doesn’t involve fungal invasion of the brain.
The advantage of this system is that the fungus and ant can both be cultured in the lab and so experiments can be done. The authors did sophisticated experiments involving infecting the carpenter ant Camponotus castaneus with the fungus, and also with a “control” fungus Beauveria bassiana, a general pathogen which doesn’t change ant behavior.
They infected ants with both fungi, and traced where the infection went with a combination of staining, producing serial sections of three parts of the ants’ bodies, staining the sections, training the microscope through “deep learning” AI to distinguish ant tissue from fungal tissue, and painstakingly putting together the sections.
In short, they found fungal tissue throughout the ant’s body, but not in the brain, even though the ants behaved as zombies. This shows that brain infection by fungal hyphae (the branching filaments that the fungus produces) is not responsible for changing the ant’s behavior.
What they did find is that in most ants the different fungal filaments connect up together to form a network, and that that network often encircles the ant’s muscles and sometimes invades them. Here’s a photo showing the hyphae joining up; the caption is from the paper. “B” shows the cross section of hyphae forming connections with each other:
Fungal interactions observed in O. unilateralis s.l.-infected ant muscles. (A) Serial block-face SEM image showing fungal hyphal bodies (HB) and hyphae (arrowheads) occupying the spaces between ant mandible muscle fibers (M). Outlined boxes are shown larger in B and C. (Scale bar, 50 µm.) (B) Connections between hyphal bodies (arrows). (Scale bar, 10 µm.) (Inset) Close-up of connected hyphal bodies. (Scale bar, 1 µm.) (C) Muscle fiber invasion: hyphae have penetrated the membrane of this muscle fiber and are embedded within the muscle cell (arrows). (Scale bar, 10 µm.)
This is a cross section, but when you put lots of cross-sections together, you can reconstruct the 3-dimensional structure of the fungal network, as in this figure (again, caption from the paper)
Three-dimensional reconstructions of fungal networks surrounding muscle fibers. (A) A single fiber of an ant mandible adductor muscle (red) surrounded by 25 connected hyphal bodies (yellow). Connections between cells are visible as short tubes, and many cells have hyphae growing from their ends. Some of these hyphae have grown along and parallel to the muscle fiber (arrowhead in Inset). This reconstruction was created using Avizo software. See also Movie S1 and interactive 3D pdf (Fig. S3). (B) Two different projections of a 3D reconstruction showing several muscle fibers (blue) and fungal hyphal bodies (red) from the same area as seen in A. This reconstruction was created using a method (developed here) that uses a U-Net deep-learning model.
The fungus not only surrounded the muscles, but in some cases penetrated the muscle fibers themselves, perhaps, the authors posit, to obtain nutrients (the generalist fungus occasionally did this, too). There is no indication that this connection of the fungal hyphae with the muscles affects how the ant behaves.
So what we have is not an answer to the question of how the zombie fungus works its magic, but how it doesn’t—through the brain. But that doesn’t mean that the behavior isn’t mediated through the brain, for the fungus could still secrete some kind of molecule that interacts with the brain and doesn’t require the fungus to enter the brain. There’s still a lot left to learn. But we shouldn’t doubt that the manipulation of ant behavior really is an evolved “extended phenotype” of the fungus.
Today’s photos are from regular contributor Tony Eales, who hails from Brisbane. Here we see nature red in, well, spores and mycelia—pathogenic killer fungi. Tony’s notes are indented:
I’ve had a few interesting sightings of late and none more so than the entomopathogenic [insect and arachnid-killing] fungi I’ve found on insects and spiders.
The first two shots are of Beauveria sp. probably Beauveria bassiana commonly called Icing Sugar Fungus. In this case it has infected a Robber Fly of the genus Ommatius.
Now the interesting thing about classifying fungi is that many have a sexual form and an asexual form, and these are so different that they have been classified as separate genera in the past. So Beauveria bassiana is the anamorph (asexually reproducing form) of Cordyceps bassiana, which is known as the teleomorph or sexually reproducing form. Both together are known as the holomorph. After 1 January 2013, one fungus can only have one legitimate name. Looking at this paper, one sees that while both Beauveria and Cordyceps are legitimate genera, for this species Beauveria bassiana would be the legitimate name.
With the next one this is a species that targets spiders. The anamorphic type Gibellula is the accepted name and the former name Torrubiella for teleomorphic forms has been deprecated.
The photos are of a small spider consumed by Gibellula cf arachnophila showing the fruiting bodies. The second is of an Arkys lancearius infected with an early stage of Gibellula and after that we see the small yellow sexual form of Gibellula cf arachnophila, formerly classified as Torrubiella sp. I collected the Arkys and have it at home in test tube in the hope it will produce fruiting bodies for me to photograph.
Last, I have an unfortunate caterpillar that has been killed by Metarhizium rileyi, another entomopathogenic fungus that is being actively investigated for its ability to kill a wide range of Lepidopteran pests. While there’s always been interest in using entomopathogenic fungi like B. bassiana and M. rileyi, the virulence of entomopathogenic fungi is affected by environmental factors such as temperature, humidity, light, and solar radiation.
You’ve probably heard about “zombie ants”: ants that become zombie-like when infected by a certain parasitic fungus. Like many parasites, some fungi can control the behavior of their hosts, and they do this to increase their own fitness, affecting the host’s morphology and behavior to make it more likely that the parasite will pass its genes to the next generation. This is simple natural selection operating on the parasite, but doing so in a way that captivates and fascinates both biologists and laypeople. How can a fungus or worm take over a larger animal and make it do its “will”? (I’m speaking in biological shorthand here.)
One of the iconic examples of such parasitism involves those zombie ants. When a carpenter ant is infected by the parasitic fungus Ophiocoryceps unilateralis(henceforth, “the parasite”), the ant’s behavior eventually changes. The parasite enters the ant through the cuticle, and then begins to grow. After 16-25 days, the fungus makes the ant climb a plant (they nest in the ground), move to a conspicuous location on a plant, and then bite down hard on a plant vein, affixing itself firmly to the vegetation. The ant dies, and the fungus grows a stalk out of the ant, ready to disperse its spores to the ground, where the infection and life cycle will resume when the fungus is encountered by the next unlucky ant.
Here’s what the dead ants with the parasite growing out of them look like:
From Wikipedia: “Ants biting the underside of leaves as a result of infection by O. unilateralis. The top panel shows the whole leaf with the dense surrounding vegetation in the background and the lower panel shows a close up view of dead ant attached to a leaf vein. The stroma of the fungus emerges from the back of the ant’s head and the perithecia, from which spores are produced, grows from one side of this stroma, hence the species epithet. . . Fungus species: Ophiocordyceps unilateralis Ant species: Camponotus leonardi doi:10.1371/journal.pone.0004835.g001
Another photo:
A dead carpenter ant with fungal spores erupting out of its head. (Image: David Hughes/Penn State University) From Gizmodo.
Clearly, the fungus is somehow manipulating the ant’s behavior to facilitate reproduction of the parasite. But how does it do this?
We don’t know exactly in any case (though there are a fair number of cases), but it must involve either growth of the parasite inside the host or chemical manipulation of a host(or both)—presumably in ways that affect the host’s brain. After all, if the brain isn’t affected, how can you modify the host’s behavior?
We now have a better, but still incomplete, idea of what’s going on with zombie ants from work described in a new paper in PNAS by Maridel Fredericksen et al. (reference at bottom and free access; pdf here). What the authors did was infect carpenter ants (Camponotus castaneus) in the laboratory with the “zombie-making” O. unilateralis fungus (as well as with a control fungus that doesn’t create zombie ants but does kill them). Then right when at the crucial moment when ant bites down on the plant, they microdissect that infected ant to see where the fungus was.
This latter procedure was a tour de force, for it involved a complex series of manipulations on a very tiny creature. The ant was dissected tiny bit by tiny bit, and then each bit was treated with immunofluorescent stain that could distinguish between fungus tissue and ant tissue. The authors then developed a computer program to look at the microscopic sections and put them together. This procedure, called “deep learning”, is a huge improvement over it being done by hand—the usual technique. As Gizmodo notes:
Using electron microscopes, the researchers created 3D visualizations to determine location, abundance, and activity of the fungi inside the bodies of the ants. Slices of tissue were taken at a resolution of 50 nanometers, which were captured using a machine that could repeat the slicing and imaging process at a rate of 2,000 times over a 24-hour period. To parse this hideous amount of data, the researchers turned to artificial intelligence, whereby a machine-learning algorithm was taught to differentiate between fungal and ant cells. This allowed the researchers to determine how much of the insect was still ant, and how much of it was converted into the externalized fungus.
What they found was surprising:
1.) First, there was no fungus in the ant’s brain, though it was present throughout the body. This really was a surprise, as everyone expected that the fungus would glom onto the ant’s brain, and that was the way it controlled its behavior. Instead, there was fungus everywhere else in the ant, especially in the muscles. (That was true of the “control” fungus, too, but, surprisingly, the paper gives no information about whether the control fungus was found in the ant’s brain).
Here’s part of a figure showing the ant’s brain (stained in green), and the nearby fungus (red); scale bar is 20 microns. There are a few fungal tracheae in the brain (arrowheads) but nowhere near the degree of intermixing of brain and fungus cells seen in muscles, and there are no fungal hyphae (the filaments of the fungus that conduct and transfer nutrients) in the brain at all, whereas they’re deep into the muscle (see below).
2.) The fungus formed a connecting network of hyphae that attached to and penetrated the ant’s muscles. Here’s an example of the networks of fungi (yellow) surrounding the ant’s muscles (red) from the paper:
(From paper): Three-dimensional reconstructions of fungal networks surrounding muscle fibers. (A) A single fiber of an ant mandible adductor muscle (red) surrounded by 25 connected hyphal bodies (yellow). Connections between cells are visible as short tubes, and many cells have hyphae growing from their ends. Some of these hyphae have grown along and parallel to the muscle fiber (arrowhead in Inset). This reconstruction was created using Avizo software.
What is the fungus doing infiltrating the muscle and forming a network that ramifies widely throughout the ant’s body? The authors posit, and this seems likely, that the fungal hyphae are sucking nutrients from the ant’s muscles and transferring them to other fungal cells not touching the muscles. This may be how the fungus feeds itself and grows throughout the ant. Muscles are rich in mitochondria, which give the ant energy reserves and are good food for the fungus. The authors also observed severe atrophy of the muscle probably connected with the fungal invasion. This muscle infiltration and formation of networks was not seen in the control fungus.
So we have two questions left:
Why does the fungus not infiltrate the brain? We don’t know, but it’s possible that doing that would quickly kill the ant and render it useless for further growth and manipulation of behavior. Further (or in addition), it may be easier to control the ant’s behavior by secreting chemicals into an intact brain than by brute-force physical invasion of the brain. After all, the behavioral manipulation by the fungus is precise: it makes the ant go to a specific exposed position on the plant (see below) and then bite down hard with its mandibles.
So how is the fungus affecting the ant’s behavior? We still don’t know. Clearly the fungal attachment to the muscles is not somehow moving the muscles in a preferred way or controlling the mandibles; rather, the muscle infiltration is a way for the fungus to get the energy it needs to grow and then form the stalk that spreads spores. What is very likely, but remains to be shown, is that the fungus secretes a chemical that somehow affects the intact brain in a way that makes the ant behave like a zombie. The authors do note that metabolite chemicals secreted by the fungus differ when it is near the brain than when it is near the muscle. Not only that, but the behavioral modification is more than just biting: the ant goes to a very specific place before biting, and that directionality somehow has to be produced by the parasite as well. As Wikipedia notes,
An infected ant exhibits irregularly timed full body convulsions that dislodge it to the forest floor. The ant climbs up the stem of a plant and uses its mandibles with abnormal force to secure itself to a leaf vein, leaving dumbbell-shaped marks on it. The ants generally clamp to a leaf’s vein at a mean height of 25.20 ± 2.46 cm above the forest floor, on the northern side of the plant, in an environment with 94–95% humidity and temperatures between 20 and 30 °C (68 and 86 °F). Infections may lead to 20 to 30 dead ants per square meter. “Each time, they are on leaves that are a particular height off the ground and they have bitten into the main vein [of a leaf] before dying.” When the dead ants are moved to other places and positions, further vegetative growth and sporulation either fails to occur or results in undersized and abnormal reproductive structures.]
In other words, the fungus has to direct the dying ant to a specific microenvironment optimal for survival and propagation of the spores.
This adds up to a real tour de force of natural selection: imagine the evolution of a chemical that can make the ant behave in such specific ways! The mind boggles: what were the intermediate steps in the evolution of this kind of host manipulation?
As Matthew emailed me (he found the paper), “What an amazing adaptation of the fungus to make the ant do the things the fungus needs it to do (‘puppet master’ is wrong metaphor because the fungus isn’t the master—natural selection is!)”. It’s stuff like this that keeps the evolutionary biologist—well, at least the ones with imagination—in a constant state of wonder and awe.
Now of course we don’t know the crucial answer: how does the manipulation of behavior actually work. But we know at least that it’s probably chemical rather than physical, and we also know that the parasitic fungus evolved adaptations for sucking nutrients from the ant’s muscles. That’s two steps forward. And the usual ending of scientific papers applies: “More work needs to be done.”
Here’s a gorgeous photo of clownfish, which just won the photographer, Qin Ling of Canada, an award in the Behaviour category at the Underwater Photographer of the Year competition (click to enlarge) – you can see all the winners here.
Ling’s photo is entitled ‘Your home and my home’. Look closely at these Nemos. Look at their mouths. Those little eyes peeking out. They are not drawn on, as PCC(E) first suggested, nor are they Photoshopped. And they are not babies. They are isopods (like pillbugs or woodlice), which are parasitic. They eat the fish’s tongue, and then replace it, sitting in there, presumably getting first dibs on the food as it comes in. They occasionally turn up on people’s dinner plates when folk order fish and get a crustacean chaser.
The photography judge said: “Six eyes all in pin-sharp focus, looking into the lens of the author … this was one of my favourite shots of the entire competition.”
Isn’t nature wonderful?
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JAC: Let me add two references and two videos. You can read Carl Zimmer’s take on these parasites at National Geographic, or Wikipedia’s entry on Cymothoa exigua, the “tongue-eating louse,” which appears to be the only species that does this.
Here’s a video, which has only one photograph:
Here’s another video with photos; it claims that this is the only case in which one organism replaces another organism’s body part:
