Readers’ wildlife photos and story: the gruesome manipulation of hosts by parasites

Fortuitously, when I hadn’t prepared any posts for today that require my neurons to work, reader Athayde Tonhasca Júnior came through with one of his patented text+photo stories, this time a fascinating one about how opportunistic natural selection can create predator/parasite niches within niches in completely unexpected and astonishing ways. This hierarchy was wonderfully expressed in the short poem “Siphonaptera” (the order in which fleas are placed) by British mathematician Augustus De Morgan:

Great fleas have little fleas upon their backs to bite ’em,
And little fleas have lesser fleas, and so ad infinitum.
And the great fleas themselves, in turn, have greater fleas to go on;
While these again have greater still, and greater still, and so on.

Athayde’s text is indented, and click on the photo to enlarge them.

The body snatchers

by Athayde Tonhasca Júnior

Family feuds abound in history and in the tabloids, but things got really out of hand with the offspring of Egyptian gods Geb (Earth) and Nut (sky). As the first-born, Osiris was naturally chosen to be the ruler of the world. But his brother Set didn’t care one bit for this undemocratic arrangement, so he decided to despatch Osiris to the Underworld. So he set out a murderous plan worthy of an Agatha Christie story. Set first commissioned a beautiful casket, tailored to fit a body with Osiris’ exact measurements. Set then organised a magnificent banquet, inviting heavenly celebrities and bro Osiris. When they were all done with the eating and drinking, Set announced a surprise. The casket was brought in, and the host told his guests that whoever could fit inside, could take it home (an odd gift to us, perhaps, but who are we to judge Egyptian gods?). One by one the guests climbed into the casket, which was too small or too big – until Osiris had a go at it. He laid down inside the casket, which, to his glee, fit him perfectly. Set’s trap was set; he slammed the casket’s lid shut and locked it, killing his sibling. Later Set retrieved Osiris’ body and chopped it into small pieces.

The Mummy (1932) escaped from his sarcophagus, but no such luck for Osiris. Art by Karoly Grosz, Wikimedia Commons:

Set’s shenanigans were the perfect inspiration for naming a new species from the genus Euderus, a small group of parasitic wasps in the family Eulophidae. Most Euderus species are moth and beetle parasitoids, but the wasp discovered by Egan et al. (2017) in Florida (USA) is peculiar, to say the least. Its host, Bassettia pallida, is itself a parasitic wasp, but of a different kind: this species is one of the many gall wasps or cynipids (family Cynipidae), which lay their eggs in oaks (Quercus spp.) and less commonly in related plants (family Fagaceae). The egg-laying induces the plant to produce a gall, which is an abnormal growth resulting from increased size or number of cells (galls can also be caused by tissue feeding or infections by bacteria, viruses, fungi and nematodes). Cynipids trigger their host plants to produce nutritious tissue inside their galls, which become ideal places for a larva to grow: there’s nothing better for one’s survival than a cosy, safe and nourishing nursery.

Oak galls or oak apples, growths resulting from chemicals injected by the larva of gall wasps © Maksim, Wikimedia Commons:

In the case of B. pallida, it induces the formation of galls inside stems of sand live oak (Q. geminata) and southern live oak (Q. virginiana). Each of these galls is called a ‘crypt’. So appropriately, B. pallida is known as the crypt gall wasp. When the adult wasp completes its development, it chews an exit hole from inside its woody quarters and flies away.

(a): a crypt gall wasp; (e): adults’ exit holes © Weinersmith et al., 2020:

Life looked good for the crypt gall wasp in the southeastern United States—until we learned about the machinations of its recently discovered enemy. The Eulophidae parasitoid locates a crypt and pierces it with its ovipositor, laying an egg inside the chamber, near or into the developing crypt gall wasp. We don’t know exactly what goes on inside the chamber, but the outcome is not good at all for the crypt gall wasp. When it tries to chew its way out, it’s no longer able to create a hole big enough to fit its body: the wasp becomes entrapped inside its crypt, Osiris-like. During its failed attempt to get out, its head blocks the exit hole. All the better for the parasitoid larva that hatched inside the crypt: it can feed at leisure on the host’s weakened body. On completing its development, the adult parasitoid wasp chews through the host’s head plug and comes out to the big wide world. So there was no better name for this species than Euderus set, the crypt-keeper wasp.

JAC: Isn’t that an amazing story? I’m sure we don’t know how the parasitoid disables the gall wasp in this way. Imagine the genetic changes involved in this complex evolution, involving the parasitoid’s egg-laying and multiple behaviors of its larval stage. But that’s a passing expression of amazement; let’s continue with Athayde’s tale:

(c): a crypt-keeper wasp pupa in a chamber made by a crypt gall wasp; (f): an exit hole plugged by the head capsule of a dead or dying crypt gall wasp; (g): a crypt gall wasp head capsule chewed through by an exiting crypt-keeper wasp © Weinersmith et al., 2020.

The relationships between oaks and these wasps are examples of host manipulation, which happens when a parasite influences the host’s behaviour or physiology to its (the parasite’s) advantage. The crypt gall wasp induces its host plants to produce galls for its benefit, and in turn the crypt-keeper wasp forces its host into becoming trapped and an easy meal for the parasitoid’s larva: the manipulation of a manipulator is known as a hyper-manipulation, an uncommon phenomenon.

A female crypt-keeper wasp, a hyper-manipulator © Egan et al., Wikimedia Commons.

There are many cases of host manipulation, and the zombie-ant fungus described by the co-author of the theory of evolution by natural selection Alfred Russel Wallace (1823-1913) is one of the better known. This fungus (Ophiocordyceps unilateralis) induces its host ants to climb up the vegetation and clamp their mandibles around a twig or leaf vein. An infected ant will stay put, rain or shine, while the fungus grows inside it. After 4-10 days the ant dies, the fungus grows a ‘stalk’ (stroma) from the ant’s head and releases spores that will infect ants walking about on the forest floor.

A dead Camponotus leonardi ant attached to a leaf vein. The stroma of a zombie-ant fungus emerges from the back of the ant’s head © Pontoppidan et al., 2009:

The more researchers look into it, the more they find cases of host manipulators such as the Darwin wasps Hymenoepimecis spp., which parasitize several species of orb-weaving spiders in the Neotropical region. A female wasp stings and temporarily paralyses her victim, laying an egg on its abdomen. The emerging larva bites through the spider’s cuticle and feeds on its ‘blood’ (haemolymph). The spider carries on with its life, building webs and catching prey, but the growing parasitoid takes its toll; eventually it kills its host.

L: A H. heidyae egg attached to a Kapogea cyrtophoroides. R: Third instar H. heidyae larva feeding on a recently killed spider; the inset shows details of the dorsal hooks used by the larva to cling to its host © Barrantes et al., 2008.

But shortly before the spider’s demise, somehow —probably by hormone injection—the larva takes command of the host’s behaviour. The spider builds a cocoon web made of thickly woven silk, which doesn’t look at all like a normal web. The spider dies, the larva enters the cocoon and completes its development. Some days later, the adult wasp emerges and flies away.

a. A normal K. cyrtophoroides web; b. The web’s hub; c. A cocoon web induced by the parasitoid; d.  Central section of the cocoon web and the wasp’s cocoon © Barrantes et al., 2008.

Parasitic wasps are not deterred by the defences of hosts such as Anelosimus eximius. This is one of the few species of social spiders; they build massive tent-like nests that shelter hundreds or thousands of individuals, who hunt together in raiding packs and even cooperate in raising their young (click the next link to watch their comings and goings). But in the Amazon region, A. eximius can’t evade the Darwin wasp Zatypota sp. A parasitized spider leaves the colony and builds its own cocoon-like web. It then becomes immobilised, so that the wasp larva can unhurriedly consume it. When finished with its meal, the larva enters the cocoon to complete its development. The larger the spider colony, the more chances of being parasitized; up to 2% of individuals become hosts to the parasitoid (Fernandez-Fournier et al., 2018).

L: A group of A. eximius in a communal web © Bernard Dupont, Wikimedia Commons. R: A 5-m long, 3-m high colony of A. eximius; photo by A. Bernard © Krafft & Cookson, 2012:.

A fierce looking H. neotropica and its larva feeding on an Araneus omnicolor © Sobczak et al., 2012.

Host manipulation seems to be much more common than we thought, so we shouldn’t expect pollinators to be safe from it. And they are not. The conopid fly (family Conopidae) Physocephala tibialis forces bumblebee hosts to bury themselves in the soil just before dying. The nematode worm Sphaerularia bombi, found throughout the northern hemisphere and South America, infects queens of several bumble bee species, castrating its host. And at least for the buff-tailed bumble bee (Bombus terrestris), the nematode also alters the bee’s behaviour (Kadoya & Ishii, 2015). An infected queen feeds normally, but does not breed or build a nest. Instead, she keeps flying into the early summer months, and by doing so she unintentionally helps to spread the nematode. Certainly many other cases of pollinators’ manipulation by parasites wait to be discovered because their effects can be subtle and inconspicuous.

CSI Garden: a post-mortem examination of a buff-tailed bumble bee found dying on a roadside pavement in England revealed an infestation by the host-manipulating nematode S. bombi © The Encyclopedia of Life:

Host manipulation can be seen as a form of extended phenotype (Dawkins, 1982; phenotype refers to a species’ observable characteristics resulting from the expression of its genes). By changing the host’s behaviour for its own benefit, the parasitoid – ultimately, its genes – expresses its phenotype in the world at large. In Dawkins’ own words, ‘an animal’s behaviour tends to maximize the survival of the genes “for” that behaviour, whether or not those genes happen to be in the body of the particular animal performing it’. The phenomenon would have deep consequences for natural selection, but the extent of extended phenotypes has been debated since the publication of Dawkins’ book.

If you are smugly assuming that behavioural puppeteering is for lower animals such as insects, you’d better think again. Some studies suggest that rodents infected with the protozoan Toxoplasma gondii become more active but sluggish in reacting to alarm signals; worse, they may become attracted to the smell of cat’s urine. If so, an infected mouse has a good chance of prematurely ending its days in a moggie’s maw – which was T. gondii‘s ‘intention’ all along, since cats are its ultimate host. And the plot thickens: infected cats excrete T. gondii spores in their faeces, which can make their way into other mammals. A 26-year study with grey wolves (Canis lupus) from Yellowstone National Park, Wyoming, USA, revealed that infected individuals – probably the result of contact with pumas (Puma concolor) – are bolder, more likely to become pack leaders and have better chances of reproducing (Meyer et al., 2022). In humans, toxoplasmosis, the infection caused by T. gondii, is widespread but usually does not have any symptoms. Most people don’t even know they have it, but all sorts of behaviour and mental disorders such as heightened aggression and Parkinson’s disease have been linked to the infection. The effects of T. gondii on rodents and humans have been disputed because data often show weak, inconclusive or no effects (Johnson & Koshy, 2020). In any case, our invulnerability to the manipulative power of parasites should not be taken for granted. Rephrasing the quote misattributed to Margaret Mead, always remember that in biology, Homo sapiens is unique. Just like every other species.

Invasion of the Body Snatchers (1956). Art by Allied Artists Pictures Corporation. Wikimedia Commons.

JAC note: I don’t think that in any of these cases of host manipulation (or any others that I’ve heard of) do we know the chemical and developmental basis of the manipulation. What does a fungus do to an ant to make it climb a stalk of grass, grip it tightly with its mandibles, and then die? How does the Darwin wasp manipulate the spider’s behavior to cause it to weave a cocoon-like web instead of its normal web—something good for the wasp? These are incredibly sophisticated manipulations that have evolved in ways we don’t understand.

If this is the work of a creator, he must have been a sadist!