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We all know that parasites are incapable of living on their own and that they depend on other living organisms for their own survival. Although symbiotic relationship between the host and the parasite is usually rare, more than one parasite may dwell in a single host. How these parasites co-exist has been studied in several host-parasite systems, but the most intriguing aspect is the strategies employed by the parasite to coax the otherwise reluctant host through behavior manipulation.
If how microscopic organisms such as bacteria and viruses can cause deadly diseases is fascinating enough, the revelation that they have the ability to manipulate the minds of their hosts for their own benefit is enthralling.
To complete their life cycle and ensure their transmission is successful, these parasites are compelled to undertake measures to make this possible. The effort the parasites are required to take to achieve this is referred to as Manipulative Effort (ME) by R. Poulin. The author believes that if the host-parasite relationship is based on costs and benefits, then natural selection will favour only those that create an ideal balance between high transmission rates and low ME costs such as host manipulation (R. Poulin, 1994)
Some parasites are known to make the host go to areas where the parasite's growth is favoured. This scenario has been observed in the case of the fungi Ophiocordyceps. unilateralis, where the fungus manipulates the behavior of ants.
Obligate parasite O. unilateralis requires worker ants for their reproduction and this becomes possible only after the growth of a large stalk, protruding from the back of the ant's head, to release the spores. Since the ant gets killed in this process, it has to die outside its colony as the other ants are quick in disposing their dead mate. This is where the infected ant's behavior is manipulated by the fungus.
Upon infection, the ant begins to behave like a zombie when it randomly walks away from its colony towards humid locations to find leaves that are ~3cm above from the ground. It bites the underside of leaves and remains attached until its death when the stalk from the head of the ant appears to release spores for subsequent infection.
None of the above characteristics displayed by the infected ant is observed in healthy ants. The random walk of the infected ants towards humid locations seems to occur only in the morning. They also seem to convulse frequently and fall down on the ground. When they bite into a leaf, the head is filled with fungal cells and their mandibular muscles are atrophied.
Although, the exact moment of death following the death-grip could not be determined, all the above distinct characteristics were observed by researchers only in infected worker ants. They are called zombie-ants as following infection; as the fungus seem to take control of the body and manipulates it accordingly in order to complete its lifecycle. (Hughes et al., 2011)
If a parasite can complete its lifecycle only in its definitive host, then it takes an indirect route to achieve this by manipulating its intermediate host in such a way that the latter is more susceptible to predation by the definitive host. This type of behavior manipulation by Toxoplasma gondii is extensively studied and observed in rodents.
Manipulation by Protozoa
The protozoa T. gondii has a very high prevalence level of 70% in cats. Members of the cat family called Felidae are the only definitive hosts of this parasite. They undergo full gametogenesis and mating within these hosts and generate oocytes that are shed in the cat's feces. If these infected feces are injested by mouse (intermediate host), the parasite can only undergo asexual reproduction. Since sexual reproduction of T. gondii can occur only in felines, the parasite manipulates its intermediate host.
Research shows that infected mice were more active and showed a preference for exposed areas unlike the uninfected mice who are usually apprehensive about exposed areas due to fear of predators. Their learning capacity was reduced and they appeared to run in circles with their head bent to one side. On the other hand, T. gondii infected rats were also found to be more active and less neophobic (fear of novelty). The exact mechanism through which this is accomplished by T. gondii remains unclear.
Interestingly, effects of T. gondii have been studied on human behavior as well. When personality tests and behavior analysis were studied between infected and uninfected human adults, significant differences were observed. The personality of infected men and women showed a decrease in novelty-seeking behavior but higher apprehension. Furthermore, it was also found that there was a high incidence of T. gondii antibodies among drivers involved in traffic accidents (Flegr, 2007). This research thus shows that, this parasite influences behavior of not only rodents but also humans.
Gut microbiota can alter emotional behaviour
Non-pathogenic gut microbiota has also been shown to alter the emotional behaviour of mice. Lactobacillus rhamnosus modulates the expression of GABA receptor expressions which play a key role in mood and anxiety disorders. It was observed that stress-induced corticosterone levels were significantly less in stressed mice that received L. rhamnosus treatment and they appeared to be less anxious. Interestingly the vagus nerve, that plays a key role for communication between the gastrointestinal tract and CNS, was found to prevent the anxiolytic and antidepressant effects of L. rhamnosus suggesting that the vagus nerve may play a role in some of the behavioural changes induced by the bacteria. (Bravo et al., 2011)
One of the factors that influence the ME of the parasite is the number of conspecifics in an individual host. In the presence of conspecifics, ME could be shared and the full cost of manipulation need not be paid by the individual parasite. However, a single parasite might be enough to induce behavioral changes. If this parasite can induce significant behavioural changes in the host that can inturn increase the susceptibility of the host, then such a parasite will be favoured by natural selection. This could lead to a race amongst them to increase or alter their ME in order to achieve transmission. (R. Poulin, 1994)
Inherited virus facilitates coexistence of wasps by behaviour manipulation
Leptopilina boulardi and Leptopilina heterotoma are competing parasitoid wasps of frugivorous Drosophila. Some females of L. boulardi are infected with an inherited virus, called L. boulardi filamentous virus (LbFV), which forces the female to lay more number of eggs in already parasitized hosts to ensure its horizontal transmission. Infected L. boulardi has a very high tendency to superparasitise the Drosophila hosts in contrast to uninfected ones or its competitor L. heterotoma. This virus appears to be specific for L. boulardi and was not observed to infect L. heterotoma which makes LbFV a strong influencing factor in the within-species competition. This study therefore suggests that the presence of LbFV reduces the competitiveness of L. boulardi, thereby facilitating the coexistence of both species (Patot et al., 2012)
Key factors that play a role in the successful transmission of a parasite are the longevity of the host and the parasite itself. If the parasite does not have a long life span or if the host has a short life expectancy then the parasite is under pressure to achieve transmission success. The parasite is then required to either manipulate the behavior of its host or wait for natural transmission opportunities. However, R. Poulin points out that natural selection will only favour those whose investments in manipulation are inversely proportional to the average longevity of the host following infection. If manipulation is not feasible, then the parasite would need to prolong the longevity of the host's life (R. Poulin, 1994).
A new virus that can make snakes tie themselves in fatal knots
Snakes, particularly boa constrictors and pythons, are affected by a fatal disease called Inclusion Body Disease. This disease is characterized by several behavioural changes in the snake such as star gazing, moving their heads back and forth and tying themselves into knots that they are unable to untie. When an arenavirus-like virus was isolated from IBD infected snakes recently, it has strengthened the previously held notion that viruses cause snake IBD. Although several aspects of this discovery remains to be studied, such as if the snakes are the natural hosts of the virus or how exactly the transmission occurs, it certainly raises the possibility that these viruses could be responsible for the unusual behavior displayed by snakes before their death (Stenglein, 2012).
Based on the above evidence of various parasites manipulating their hosts we can say that they strictly maintain a cost-benefit relationship with their hosts, irrespective of the latter's involvement or resistance. Since natural selection chooses only those who seem to achieve transmission success, several strategies are employed by the parasites including behavior manipulation. However, the type or amount of manipulative effort invested by the parasite varies widely between different host-parasite systems and is indeed very interesting to study and observe.