By Vidya Rajan, Columnist, The Times
We act, we think, rationally. But our thoughts are subject to manipulation: by new ideas, new experiences, psychoactive drugs, and … parasites.
Parasites are organisms that take up residence in a host, and then proceed to use the host’s energy to replicate themselves and spread. If the host is killed as part of the process, then the parasite must find some way to leapfrog into another host’s body, or else it will die when the host does. When the method involves the host dying, something that the host is probably not very keen to do, the parasite must change the host’s behavior, making it take risks that are laser-focused at increasing the parasite’s chances of dissemination. Other behaviors are less an existential risk for the host and may cause them to sneeze or bite or defecate, placing the parasite in a position to infect a new host.
How to manipulate? Animal minds are a collection of neurons that communicate using chemical signals called neurotransmitters. A single neuron is a cell, a ganglion is a cluster of neurons, and a brain is just a larger cluster. All of them talk through chemical signals. A parasite needs only to control the signalling to manipulate the brain and the behavior. It is not as if the parasite knowingly targets a specific behavior; the process of evolution means that many hundreds or even thousands of parasites infecting a host may produce slightly variable signals targeted to slightly different areas of the host’s brain.
Only the parasites that unknowingly produce an effective signal will survive, but, and here is the key to success: the offspring of parasites that succeed will inherit that signal from their successful parents. Sequential rounds of what Darwin termed “natural selection” will finesse the parasite-host relationship to optimize the parasite’s control of host behavior. Just because we are seeing the results of thousands of generations of selections doesn’t mean that the parasite started off with such exquisite manipulation of host behavior. It would be the same as looking at a high-performance car like a Lamborghini, and thinking that it had just sprung into existence in a single step. It wouldn’t be true: cars started off a slow and inefficient jalopies, and were honed to better performance through many iterations and design modifications; so are parasites that control minds. Another thing: it’s not only animals with neurons that can be manipulated. Evidence shows that plants can be manipulated by plant parasites as effectively as animals can be manipulated. In this article, I will survey some of the more outlandish examples of parasitic manipulation of hosts.
A recent excellent article in Bee Culture by Jay Evans (September 2020 issue, page 36) described many of the parasites that exert such host mind control. Some of the examples Jay described in the article were fungi that cause ants to climb high on a plant and then die, becoming a vessel for the production of spores that rain down on the forest floor and infecting ants that crawl about below; grasshoppers who try briefly and vainly, at the urgings of parasitic hairworms inside them to swim, providing the perfect aquatic environment for the hairworms to emerge and reproduce; the parasite Toxoplasma gondii, which eliminates the natural fear that mice have for cats in which the parasite reproduces. There are a plethora of others not mentioned in the article, probably for lack of space: the rabies virus which causes its host to froth and foam and bite, a bite which transfers rabies virus into new hosts; tapeworm eggs in bird droppings eaten by fish, which grow into adult tapeworms that cause the fish to become reckless and emerge into the open where they immediately get preyed on by birds whose droppings will later contain eggs which will begin the fish-bird infection cycle anew (phew – that was a long sentence); guinea worms which emerge with painful burning from the lower limbs of infected people causing them to seek water bodies to ease the burning, and into which the worm will deposit its eggs to infect future hosts who drink the contaminated water; snails which harbor a parasite that make the snail flash its antennae and attract a bird’s attention to get eaten to complete their life cycle. And many more I don’t have space for in this article…
Parasite infections, specifically of insects, can be classified into three groups [1] and summarized as: 1. Behavior manipulations that cause the host to die in ways that favor parasitic dissemination to another host; 2. Those that force the host to become guards to the parasite; 3. Those that affect the ability or motivation for movement.
Behaviors that cause the host to become a disseminator of the parasite include ants infected with Lancet liver flukes (Dicrocoelium dendriticum) that need to complete their lifecycles in grazing animals and snails. The flukes enter the brain of ants which then climb to the top of grass stalks and clamp on with their jaws. Animals like cows then consume them and the fluke travels into the liver and matures, releasing eggs that are expelled with the feces. Snails consume the droppings and the fluke eggs, which hatch into larvae inside the snails. Snails expel the larvae encased in slime balls, a food for ants, and the fluke matures inside the ant and travels into the hemolymph and up to the sub-oesophageal ganglion where its secretions drive the ant, at dusk, to leave the nest and climb to the top of a blade of grass to initiate another cycle of infection. Even more remarkable is the parasitic gall wasp, Bassettia pallida, that causes galls to form in oaks. These oak galls host the developmental stages from eggs through pupae of the gall wasp, which later emerges from the crypt. However, the parasitic gall wasp can itself become host to another wasp, the parasitic crypt-keeper wasp, Euderus set. The keeper wasp lays eggs either in the crypt or on the parasitic gall wasp, and, upon metamorphosis, the parasitic gall wasp cuts open the crypt, but then plugs the hole with its own head and dies. The crypt-keeper wasp offpsring then mature inside the crypt and exit through the head of the parasitic gall wasp that so conveniently saved them the trouble of excavating a chamber to develop inside.
In the cases of the host becoming a protector of the parasite, there can be fairly mundane or truly horrifying outcomes. The ant Pristomyrmex punctatus receives a sweet secretion laced with dopamine from the caterpillar Narathura japonica. This causes the ant to become quite aggressive in protection of the caterpillar as its food source, but the caterpillar does not otherwise impact the ant’s life or offspring. More grim is the life of the ladybug, Coleomegilla maculata, infected by the wasp, Dinocampus coccinellae. The wasp lays its egg inside the ladybug, but there is a virus inside the egg which makes its way to the ladybug’s nervous system. The egg hatches, and the larva emerges from the ladybug and takes up residence between the ladybug’s legs where it spins a pupa. Simultaneously, the virus in the ladybug’s nervous system starts replicating, causing a neuropathy which makes the ladybug twitch and rear. These actions of the ladybug scare off predators that might otherwise eat the pupa. The wasp emerges and leaves, and the ladybug, its protective services no longer needed, dies. The most gruesome of the protector zombies is the caterpillar, Thyrinteina leucocerae, which is parasitized by a wasp of the Glyptapanteles species. The wasp lays many tens of eggs inside the caterpillar which behaves normally although it is being eaten from the inside until the larvae are ready to pupate. Then all but one or two larvae pupate, piercing through the caterpillar’s body. However, the caterpillar is still alive, and the larvae inside cause the caterpillar to rear and thrash should a predator, such as a bird, come near. The actions protect the pupae until they develop into wasps. The caterpillar, its job complete and perforated like a sieve, dies.
Then there are a multitude of mind-altering insect parasites, some of which exhibit grisly behavior worthy of an alien body-snatching movie. My personal gory favorite is the emerald wasp, Ampulex compressa, which hijacks the body and the mind of the cockroach [2-4]. The wasp stings the cockroach precisely in the prothoracic ganglion which paralyze the legs of the cockroach and prevents its moving. Then the wasp injects a venom directly into the brain and sub-esophageal ganglion which contains the neurotransmitter dopamine, which induces the cockroach to groom itself for about 30 minutes, possibly as a way to both clean off the body surface that the wasp will lay its egg on, and also to keep the cockroach immobilized while the wasp digs a burrow. After grooming, the cockroach enters a state called hypokinesia characterized by lack of escape response and mechanical walking. The wasp then deposits an egg on the cockroach abdomen, and then leads the cockroach by its antenna to its burrow wherein it entombs the living cockroach with the egg. The egg hatches into a larva that burrows into the host, eating its insides in a carefully calibrated manner so the cockroach stays alive as long as possible. The cockroach, as it is being hollowed out by the larva, does not attempt escape; instead it docilely lets itself be eaten until it dies around day 8. The wasp larva then pupates and emerges as an adult in a month.
Beekeepers know of the North American native Apocephalus borealis wasp which deposits eggs in honeybee, bumblebees and paper wasps. The larvae emerge inside and eat the honeybee from the inside. Bees infected by the wasp behave abnormally. They fly out of their hives and towards light sources and are often found crawling around on the ground near lamps or porch lights. The weakened bee usually dies, but, within 5-14 days, larval grubs or pupae emerge from the thorax of the bee. The ZomBee projects asks for your help in identifying regions of the United States that the wasp is present in, but also where the wasp is absent. If you want to help with this citizen science project, go to ZomBeeWatch.org
A curious common thread is the use of the hormone dopamine which reinforces motivation and learning via the reward pathway [5]. That is, dopamine makes one want to do something because it feels good. If the poor dopes are getting duped by dopamine hits that make them feel good for being eaten alive from the inside out, well, at least they are getting something out of it.
- Libersat, F., M. Kaiser, and S. Emanuel, Mind control: how parasites manipulate cognitive functions in their insect hosts. Frontiers in psychology, 2018. 9: p. 572.
- Moore, E.L., et al., Ampulexins: A new family of peptides in venom of the emerald jewel wasp, Ampulex compressa. Biochemistry, 2018. 57(12): p. 1907-1916.
- Haspel, G., L.A. Rosenberg, and F. Libersat, Direct injection of venom by a predatory wasp into cockroach brain. Journal of neurobiology, 2003. 56(3): p. 287-292.
- Gibson, J., et al., Eclosion of Physocephala tibialis (say)(Diptera: Cnopidae) from a Bombus (Apidae: Hymenoptera) host: A video record. The Journal of the Entomological Society of Ontario, 2014. 145.
- Berke, J., What does dopamine mean?(2018). Nat Neurosci, 2018. 21(6): p. 787-793.
