Adapted from Venomous: How Earth’s Deadliest Creatures Mastered Biochemistry, by Christie Wilcox, by arrangement with Scientific American/Farrar, Straus and Giroux, LLC (US), Bungeishunju Ltd. (Japan). Copyright © 2016 by Christie Wilcox.
I don't know if cockroaches dream, but i imagine that if they do, jewel wasps feature prominently in their nightmares. These small, solitary tropical wasps are of little concern to us humans; after all, they don't manipulate our minds so that they can serve us up as willing, living meals to their newborns, as they do to unsuspecting cockroaches. It's the stuff of horror movies, quite literally; the jewel wasp and similar species inspired the chest-bursting horrors in the Alien franchise. The story is simple, if grotesque: the female wasp controls the minds of the cockroaches she feeds to her offspring, taking away their sense of fear or will to escape their fate. But unlike what we see on the big screen, it's not some incurable virus that turns a once healthy cockroach into a mindless zombie—it's venom. Not just any venom, either: a specific venom that acts like a drug, targeting the cockroach's brain.
Brains, at their core, are just neurons, whether we're talking human brains or insect brains. There are potentially millions of venom compounds that can turn neurons on or off. So it should come as no surprise that some venoms target the carefully protected central nervous system, including our brains. Some leap their way over physiological hurdles, from remote injection locations around the body and past the blood-brain barrier, to enter their victims' minds. Others are directly injected into the brain, as in the case of the jewel wasp and its zombie cockroach host.
Making of a zombie
Jewel wasps are a beautiful if terrifying example of how neurotoxic venoms can do much more than paralyze. The wasp, which is often just a fraction of the size of her victim, begins her attack from above, swooping down and grabbing the roach with her mouth as she aims her “stinger”—a modified egg-laying body part called an ovipositor—at the middle of the body, the thorax, in between the first pair of legs. The quick jab takes only a few seconds, and venom compounds work fast, paralyzing the cockroach temporarily so the wasp can aim her next sting with more accuracy. With her long stinger, she targets her mind-altering venom into two areas of the ganglia, the insect equivalent of a brain.
The wasp's stinger is so well tuned to its victim that it can sense where it is inside the cockroach's dome to inject venom directly into subsections of its brain. The stinger is capable of feeling around in the roach's head, relying on mechanical and chemical cues to find its way past the ganglionic sheath (the insect's version of a blood-brain barrier) and inject venom exactly where it needs to go. The two areas of the roach brain that she targets are very important to her; scientists have artificially clipped them from cockroaches to see how the wasp reacts, and when they are removed, the wasp tries to find them, taking a long time with her stinger embedded in search of the missing brain regions.
Then the mind control begins. First the victim grooms itself, of all things; as soon as the roach's front legs recover from the transient paralysis induced by the sting to the body, it begins a fastidious grooming routine that takes about half an hour. Scientists have shown that this behavior is specific to the venom, as piercing the head, generally stressing the cockroach, or contact with the wasp without stinging activity did not elicit the same hygienic urge. This sudden need for cleanliness can also be induced by a flood of dopamine in the cockroach's brain, so we think that the dopaminelike compound in the venom may be the cause of this germophobic behavior. Whether the grooming itself is a beneficial feature of the venom or a side effect is debated. Some believe that the behavior ensures a clean, fungus- and microbe-free meal for the vulnerable baby wasp; others think it may merely distract the cockroach for some time as the wasp prepares the cockroach's tomb.
Dopamine is one of those intriguing chemicals found in the brains of a broad spectrum of animal life, from insects all the way to humans, and its effects are vital in all these species. In our heads, it's a part of a mental “reward system”; floods of dopamine are triggered by pleasurable things. Because it makes us feel good, dopamine can be wonderful, but it is also linked to addictive behaviors and the “highs” we feel from illicit substances like cocaine. It's impossible for us to know if a cockroach also feels a rush of insect euphoria when its brain floods with dopamine—but I prefer to think it does. (It just seems too gruesome for the animal to receive no joy from the terrible end it is about to meet.)
While the cockroach cleans, the wasp leaves her victim in search of a suitable location. She needs a dark burrow where she can leave her child and the zombie-roach offering, and it takes a little time to find and prepare the right place. When she returns about 30 minutes later, the venom's effects have taken over—the cockroach has lost all will to flee. In principle, this state is temporary: if you separate an envenomated roach from its would-be assassin before the larva can hatch and feed and pupate, the zombification wears off within a week. Unfortunately for the envenomated cockroach, that's simply too long. Before its brain has a chance to return to normal, the young wasp has already had its fill and killed its host.
The motor abilities of the roach remain intact, but the insect simply doesn't seem inclined to use them. So the venom doesn't numb the animal's senses—it alters how its brain responds to them. Scientists have even shown that the stimuli that normally elicit evasive action, such as touching the roach's wings or legs, still send signals to the animal's brain; they just don't evoke a behavioral response. That's because the venom mutes certain neurons so they are less active and responsive, leading to the roach's sudden lack of fear and willingness to be buried and eaten alive. This venom activity requires toxins that target GABA-gated chloride channels.
GABA, or γ-aminobutyric acid, is one of the most important neurotransmitters in insect—and human—brains. If neuron activity is a party, then GABA is a wet blanket; it dampens a neuron's ability to be triggered through activation of chloride channels. When chloride channels open, they allow negative chloride ions to flow. Because these ions like to hang out with positive ions, if these channels are open when a sodium channel happens to open, chloride ions can cross the membrane at almost the same pace as sodium ions, making it harder for the sodium ions to start the domino cascade that is neuron signaling. Even though a neuron receives the “go” command, the action potential is stopped in its tracks. GABA isn't a complete inhibitor, however—the chloride channels can't wholly keep up with the sodium channels, so a strong stimulus can overcome the dampening effect. This dulling system is what the wasp co-opts to make the cockroach do her bidding. Her venom is packed with GABA and two other compounds that also activate the same chloride receptors, β-alanine and taurine. These also work to prevent the reuptake of GABA by neurons, prolonging the effect.
Although these venom compounds can cut the brain activity that would make her prey flee, what they can't do is make their way to the right parts of the cockroach brain by themselves. That's why the wasp has to inject them directly into the cockroach's ganglia. Fortunately for her, in a convenient quirk of nature, the same venom that zombifies roach brains works like magic to produce the transient paralysis needed to line up the cranial injection. GABA, β-alanine and taurine also temporarily shut down motor neurons, so the wasp only needs one venom to complete two very different tasks.
With her prey calm and quiescent, the wasp can replenish her energy by breaking the roach's antennae and drinking some sweet, nutritious insect blood. Then she leads her victim to its final resting place, using what remains of an antenna as an equestrian uses the reins on a bridle. Once inside her burrow, she attaches one egg to the cockroach's leg, then seals her offspring and the roach in.
As if the mind manipulation wasn't bad enough, the wasp's venom has one final trick. While the roach awaits its inevitable doom, the venom slows down the roach's metabolism to ensure it lives long enough to be devoured still fresh. One way metabolism can be measured is by how much oxygen is used up over time, as all animals (including us) use oxygen in the process of creating energy from food or fat stores. Scientists have found that oxygen consumption by cockroaches that have been stung is much lower than that of their healthy roach friends. They thought this might be the result of the reduced movement of the complacent victims, but even when paralysis is induced by using drugs or severing neurons, the stung cockroaches live longer. The key to the prolonged survival seems to be hydration. How exactly the venom acts to keep a roach hydrated is not known, but it ensures that when the wasp larva hatches from its egg, its meal is ready to eat. And soon enough after that, a new wasp emerges from the burrow, leaving the roach carcass behind.
Jewel wasp venom is only one example of neurotoxic venom taken to the extreme. There are more than 130 species in the same wasp genus, including the newly described Ampulex dementor (named for the soul-sucking guards of the magical prison Azkaban in the Harry Potter series). Ampulex belongs to a very large and diverse group of wasps, numbering at least in the hundreds of thousands of species, which are known for some serious mental manipulation. All have a macabre life cycle: as adults, they feed like other wasps and bees, but as larvae, they must feed off other animals. They're not quite independent, not quite parasites—they're parasite-ish, or as scientists call them, parasitoids.
Cockroaches are not their only targets; there are parasitoid wasps that lay their eggs in spiders, caterpillars and ants. The temperate Northern Hemisphere wasp Agriotypus will dive underwater to attach her eggs to caddis fly larvae and can remain submerged for up to 15 minutes to accomplish her task. The brave Lasiochalcidia wasps of Europe and Africa throw themselves into the nightmarish jaws of an ant lion, pry them apart and insert their eggs into its throat. There are even wasps called hyperparasitoids that parasitize other wasps like themselves, such as Lysibia species of Europe and Asia, which will sniff out caterpillars parasitized by fellow parasitoid wasps in the genus Cotesia and lay eggs in the freshly pupated wasp larvae. In some cases, multiple wasp species parasitize one another, leading to a Russian doll of parasitic interactions.
And to ensure their safe passage from larva to adulthood, these wasps often gain more than just a meal from their hosts. One of them turns its caterpillar hosts into undead bodyguards that will defend pupating young wasps that just ate through its body. Another species' larva forces its spider host to spin it a deformed but durable web to protect its cocoon just before killing the arachnid.
Whereas the wasps in this unusual family may have perfected the art of mind control, there are other venomous species whose toxins alter mental states. There are even species whose neurotoxic compounds get through our own blood-brain barrier, a feat that no wasp venom can yet achieve. But unlike cockroaches, we Homo sapiens have a strange affinity for substances that mess with our minds. Although the roaches run from those that would twist their brains, some people are willing to pay upward of $500 for a dose of venom to have a similar experience.