Parasites Affecting Insect Behaviour

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1) Infected Cephalotes ant.

Parasites need to have adaptations for colonisation, defeating immune systems and transmission. Often, parasitism involves very complex interactions between not-so-closely-related organisms. For example, the jungle-dwelling turtle ant above is infected by nematodes that gather and mate in the gaster (hind part of the ant). They deteriorate the cuticle of the gaster (turning it red), as well as the petiole joint (which joins the gaster to the rest of the ant). Not only that, they somehow mess around with the ant’s brain, making it stay on top of trees and wave its gaster around. The only reason for this is to make the ant’s gaster attractive to birds: they look like fruit and are swinging around, asking to be eaten; the nematodes need the birds to complete their life cycle.

2) Scale insect

Parasitism can be seen as a form of symbiosis, when symbiosis is viewed as a continuum. At the one end, you have obligate symbiotic relationships such as bacteria living in a cow’s stomach. On the other end, you have pathogenic parasites that infect and kill their hosts in order to eat their corpses. However, there are no sharp lines dividing these categories; it’s more of a gradient. As an example, consider scale insects. They live in colonies endemically on plant leaves (some may see them as plant parasites). A few individuals can get infected by the fungus Septobasidium, which kills those individuals and builds a whole coccoon over the leaf, trapping the insects inside. However, this is perfect (for everyone but the plant): the insects are guaranteed reproductive success and protection from other pathogens, while the fungus gets a free source of food. It’s both symbiotic in the way the scale insects and the fungus cooperate, but the way this cooperation starts is parasitic.

Some advantageous symbionts may turn pathogenic under certain conditions – this is one of the models for the evolution of parasitism. The degree of adaptation and specialisation that parasites have indicates that they must have been in a close relationship with their hosts, as symbiotic organisms. Other times, the parasite doesn’t affect its host and only uses it as a vector (mosquitoes and Plasmodium, for example). The fact that many hosts and vectors have special compartments for their parasites, especially if they are beneficial, is also a strong indication that regular symbiosis was at the start of a parasitic relationship.

3) Selected strepsipteran life cycles

The picture above shows just how complex parasitic life cycles can get, using the example of the strepsipterans, a group of obligately parasitic insects. I will not go into detail about them because they deserve a blog post on their own, but the complexity of parasitic interactions should never be underestimated. Especially when speaking of entomopathogenic fungi, just talking of the mushroom and its host insect is nowhere near enough. All the evidence points to tritrophic interactions between plant, insect and fungus. The most plausible theory of the evolutionary origin of fungi that infect insects is that they were originally plant pathogens. There are many dimensions to parasitism, and while some cases are really simple, the majority are deceptively simple.

Parasitism involves a kind of physiological race. All organisms have an immune system, which a parasite has to overcome. Generally, there are two ways. The first is stealth. Instead of making their presence known, they may cloak themselves in a suit that is molecularly very similar to their host, so that the immune system doesn’t recognise them. On the other hand, there are aggressive parasites that actively suppress their host’s defences or are simply genetically resistant.

To give a glimpse into the nuances of parasitism, let’s look at how parasites can affect their hosts, and since deadly ones are the coolest, we’ll look at those. A parasite’s survival depends on it finding its particular host, and as the nematode example at the beginning shows, they can go to extreme and convoluted measures. But sometimes the effects are subtle and to really drive this point home, we’ll use suffering children: Plasmodium, the malaria-causing parasite, is transmitted to humans via mosquitoes. In the human, it multiplies (causing malaria and eventually death), but if it were to stay within one body, it’s useless for its survival. What Plasmodium does, however, is attract mosquitoes to infected humans, possibly by releasing attractants, and further propagating the species – this is why infected people get bitten much more than uninfected ones. Plasmodium also acts when in the mosquito: those carrying Plasmodiums tend to sting more than those not carrying the parasite.

4) Medicinally important parasites and their life inside the host. a-e: Plasmodium (Malaria); Trypanosoma brucei gambiense (Sleeping sickness); Leishmania (leishmaniasis); Wuchereria bancrofti (river blindness); Dengue fever virus.

Similarly, Leishmania, the protozoan causing leishmaniasis, manipulates its sandfly vector to bite humans more than usual. It secretes a gel in the sand fly’s gut, blocking it and limiting how much food (blood) it can extract in one go, so the sandfly has to feed more times. Every time it feeds, some more parasites escape into the human. As the picture above shows, there are other nasty disease-causing parasites that rely on insects for their life cycle, so investigating their effects on the insect host is of paramount importance to the medical community.

5) Aphids

To use less morbid examples, the fungus that causes Dutch elm disease makes the trees produce volatile compounds that attract bark beetles, which act as the fungus’s intermediate host. Similarly, the barley yellow dwarf virus makes infected barley plants much more attractive to aphids than uninfected barley plants.

The transmission mode of these pathogens can be seen as somewhat passive, even though they do influence their hosts’ behaviour. But they don’t force their vectors, they just make themselves unknowingly attractive: birds see a colourful ant gaster and eat it thinking it’s a fruit; aphids swarm on an infected plant because it smells good. They aren’t being specifically guided to spread the parasite. But wouldn’t it be cool if there were parasites that directly affected their hosts?

Luckily, nature is awesome (in both the literal and the colloquial meaning). Behaviour ultimately boils down to changes in neurochemistry in the brain. Therefore, common sense tells us that it’s not really surprising that there are simple ways in which parasites can directly affect their host’s behaviour: it’s simply a matter of the right molecules in the right place.

6) Jewel Wasp with a cockroach

Let’s look at the case of the jewel wasp, a cockroach parasite. Jewel wasp larvae feed on live cockroaches, but they’re far too small to hunt them themselves. What happens is that the adult female wasp stings a cockroach, injecting it with neurotoxins. They don’t kill the roach, nor do they paralyse it. They make it lose its ability to walk wherever it wants. This allows the wasp to lead the cockroach to its nest, where it lays an egg on it. The larval wasp emerges and eats the live cockroach, who doesn’t run away or even fight back – because of the neurotoxins.

The wasp is clever and knows exactly where to sting the roach in the head, namely in the supra- and subesophagal ganglia, and they are more precise with their sting than any brain surgeon. While walking is controlled by the thoracic ganglia, it’s in the brain that the signal originates – where to go, how fast, etc – and that’s what the wasp disables. In effect, the roach loses its free will. When specifically stimulated, it will still move – it can still swim, fly, move its antennae and sense its environment. It just doesn’t want to walk. There are other examples using other insect hosts (crickets, grasshoppers).

7) Transmission of parasite in social insects.

This is a charming life cycle and an excellent example of a parasite hijacking its host. But when you look at it, it does seem a bit subdued: the roach isn’t possessed, it’s merely drugged. This is understandable, since a parasitic wasp only needs a single cockroach for a single larva – no need for excess. Parasites that infect eusocial insects have a whole world of opportunity open to them: ants, for example, live in densely-packed colonies and come into contact with each other all the time, and all of them are practically clones. An ant pathogen can potentially have all of them as hosts – just see the diagram above to see how easy it theoretically is. A parasite enters the colony (2), gets established (3) and spreads quickly due to the genetic similarity and close contact of the ants in a nest (4). And from there, it’s simple to jump to another colony (5).

8) Temnothorax

Unfortunately for the pathogen (we’ll use Metarhizium for now), ants are very smart. An infected ant will often go away from the colony to die alone, quarantining itself to save the colony. Or is it? Another explanation is that the fungus is controlling the ant to move away from the nest in order to have the chance to infect other colonies. It may sound a bit exaggerated, but the fact that these infected ants stand on top of grass stems to die is perfect for the spread of fungal spores (by wind).

But no, it is in fact a completely independent decision by the ant to die for the greater good. They completely abandon the nest, cut off contact with their mates and stop foraging for food. If, under experimental conditions, they are placed back in the nest, they get thrown out. In contrast, sick individuals (not infected) get treated and cared for. It’s an active, group-level adaptation against fungal pathogens, much like the suicidal sting of a honey bee protects the entire colony at the cost of one individual. In fact, all social insects have this social immune system – and not just a behavioural one. There are also ‘medicines’ produced and all that, which I will not detail.

There are some species with very large colonies that build specialised compartments (‘hospitals’, ‘morgues’) where the infected individuals can go and die, and get cleaned up by a special subcaste. But this can only be observed in the largest colonies that can afford a few losses in case something goes wrong.

Another very important note, especially concerning this next section: interpreting whether a parasite is directly manipulating its host is very tricky; sticking insects in an MRI doesn’t work, and there must always be a distinction made between direct control and simply a passive side-effect of infection. While it is tempting to say that a specific effect is evolutionary adaptive to the parasite, such a conclusion is necessarily speculative, since in most cases, we can’t know just how far the parasite is controlling the insect.

Take hairworms for example. They infect land-living arthropods and cause them to jump into rivers and drown, thereby releasing the aquatic adult hairworm. It’s very tempting to say that the hairworm was driving the arthropod, but without neurological studies, we cannot say this for sure. The hairworm is definitely affecting its host’s behaviour, and it’s doing so to its advantage, but to say that it is in control of its host’s behaviour is a stretch: those chemicals it is releasing may only be inducing a sense of thirst, not a desire to swim. This would fit with the general observation that parasites always mess around with hormone and other endocrine systems; direct neurological hits are rare.

There is, however, a different parasite that does directly control its host: Dicrocoelium dentriticum, a trematode. It makes an ant climb up a blade of grass so that a cow will eat it. The difference between this one and Metarhizium is that Dicrocoelium actively takes over the ant’s navigational system. What happens is that after the ant ingests them (the cow shits them out, snails eat the feces and eject them in slime balls, which the ants then eat), they remain passively floating around the hemocoel (‘bloodstream’). At a random point, all the parasites turn into cysts. Except for one! It goes directly to the subesophagal ganglion and takes over the ant at night, making it go up the blade of grass. If the ant is not eaten by daytime, the parasite releases its grip and the ant goes about its day normally, until night falls again. Here you have a parasite that is directly manipulating its host.

9) Adult Maculinea

Another life cycle, again with ants, but this time involving one more parasitic level. The caterpillar of the above butterfly is an ant parasite, living in their nests and getting the ants to care for it by releasing specific chemicals that make the ants think it’s one of them. However, the caterpillar also happens to be the host for a parasitic wasp, and the wasp must get to it somehow. It releases other chemicals that make the ants fight each other, and the wasp can just stroll through the nest unharmed and infect the caterpillar.

10) Plesiometa

Staying with parasitic wasps, take the spider above. It gets parasitised by a wasp that stings it once, paralysing it and laying an egg on its back. The spider eventually recovers and goes on living completely normally, while the larva stays on its back, feeding off its hemolymph. But then, right before the larva kills the spider, the spider spins a very special web – one that’s perfect for supporting the wasp’s coccoon, especially in the rain. The wasp larva kills it and goes into the web that the spider built for it and pupates.

This brings us to evolutionary theory. It seems as though all these parasite-host interactions are beneficial to the parasite, so much so that the host’s behaviour can be seen as the parasite’s extended phenotype (not sensu Dawkins, 1982!). One ant may die, but the fungus can spread all over the landscape. To look at this more closely, we’ll bring in Ophiocordyceps, arguably the most famous insect parasite (it’s the zombie ants one).

In case you haven’t seen the David Attenborough video, here’s a quick recap. Ophiocordyceps is a fungus that infects ant. It’s highly specific (one species for one ant). Once in the ant, it controls its behaviour so that the ant bites its way to the top of a leaf, facing the wind and off the ground and dies. The fruit body (‘mushroom’) then grows out of its head and its spores are spread.

11) Cross section through an Ophiocordyceps-infected ant.

What the cross section section above shows is that the fungus isn’t just growing randomly and colonising every possible space inside the ant. It’s specific and organised. This ‘knowledge’ that the parasite has also extends to the actual ant. An infected ant doesn’t immediately show symptoms, as the fungus only feeds on unimportant organs. It goes about its life, foraging and eating. The fungus strikes when all the useless stuff has been eaten from the ant. The ant will then go through the usual death grip as the fungus eats its brain. It will position itself exactly where the parasite wants; experimentally moving a dead ant away completely destroys the fungus’s spread. The ant will not go into environments that are detrimental to the fungus (too warm, cold, not enough humidity, etc). When the ant dies, it bites into the largest vein of a leaf (again, instructed by the fungus), so that there is a continuous source of food for the fungus (the fungus then grows all around the ant to prevent it from falling off). Cordyceps‘s ‘prized’ medicinal properties also derive from its lifestyle: it produces antibiotica to stop bacteria and other animals from growing on it or the ant, securing all the nutrients for itself.

The best way to explain such a tight relationship between the Ophiocordyceps and the ant is by saying that the ant represents Ophiocordyceps‘s extended phenotype; the parasite, in this case, really has complete control over its host and knows exactly what to do with it. The evolution of this is still a mystery, but the fact that it is found in fossils also (pers. comm., in press) hints that it’s been there for awhile and may have been originated from some kind of coevolutionary race: the pathogens that can get the most out of their hosts get selected for, while those hosts that can avoid/get rid of their pathogens are at an advantage.

Sticking with insects, besides having a regular immune system, a large part of their defence is behavioural, i.e. avoiding coming into contact with pathogens (assuming they are visible, like fungi). An excellent example is grooming: if an insect senses spores on its cuticle, it will groom itself as a defensive response meant to throw away the spores. The fungus may then react (in an evolutionary sense, not actively) by either making smaller spores, so the insect doesn’t feel them, or by making itself somehow attractive (releasing pheromone-like chemicals, for example).

12) Termite

These behavioural responses have mostly been studied in an agricultural context, since fungal pathogens can potentially make excellent biological pest control agents. To use a concrete example, termites are a large nuisance. When they detect a pathogen in the soil, they dig a tunnel, stuff the fungus in there and seal it off, making it useless to use against termite populations. A possible solution would be to artificially put the fungal spores inside tasty capsules. But even then, you have to deal with the social response. Infected termites don’t generally leave the nest; however, they are treated by their fellow termites (by grooming and biting) and if they are not cured, they are buried to prevent the fungus from spreading; any spores lying around can be eaten safely without risk. So while there may be natural entomopathogens, using them purposely for biological control is tricky and not as simple as it sounds.

13) Popillia larva

The best solution for any insect is to simply avoid the pathogen (better safe than sorry). For example, the larva above is a plant pest and is also susceptible to infection, but actively avoids going near any potentially dangerous fungus. So a solution (that works) is to simply infect the important area, and the pests will not come.

But before you all go off thinking pathogens are awesome, remember that this post was extremely biased and that the majority of pathogenic spread is more or less by chance; only those that are specialised and adapted to a very specific life cycle have these elaborate mechanisms. There’s no doubt that we will find more of them that directly manipulate their insect hosts, but the proof is hard to get and it is very easy in these cases to confuse causation and correlation. No matter what kind of chemical cocktail parasites release into their hosts (and they are a lot, and can even include virals and teratocytes), it is imperative not to exaggerate what are mere accidents and side effects, while recognising when genuine manipulation is taking place.

References and Further Reading

Image Sources

  1. Hughes et al., 2008
  2. Ángel Hernansáez
  3. Kathirithamby, 2009
  4. Hilary, 2003
  5. Aphidman
  6. Radio Ga Ga
  7. Cremer et al., 2007
  8. IES-MGB
  9. camerar
  10. RABTOR
  11. Andersen et al., 2009
  12. ralfbucana
  13. meeyauw