Neuroethology of Parasites That Alter Host Behaviour

Zombies
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The popular culture phenomenon of "zombies" becomes a reality as
science unveils the mysterious "zombifying" agents of nature.
How to Look Like a Zombie [Photograph]. (n.d.). Retrieved
March 28, 2013, from: http://www.wikihow.com/Look-Like-a-Zombie.

Neuroethology is the study of the functions of the nervous system and the resulting animal behaviour using an evolutionary approach. Recently, the biotic interactions that lead to behavioural changes in an organism have become a topic of great interest. The research of infections that induce behavioural changes is translating the enigmatic phenomenon referred in science fiction as ‘zombies’ into real science. Though some details of the drama observed in zombie apocalyptic films do not accurately depict what is occurring in the wild, the subtlety and intricacy of behaviour-altering interactions in nature are astonishing. Current data on parasites that cause changes in host behaviour suggest that such interactions may be more ubiquitous in nature than previously imagined. In many cases, parasites that turn their hosts into ‘zombies’ have complex lifecycles in which different species serve as hosts at different stages of parasite ontogeny. As with studying any interaction between organisms, such as predation, competition, and mutualisms, the evolutionary history of these charismatic interspecific interactions must be considered to infer the coevolutionary dynamics that persisted over millennia or perhaps even millions of years.

Neurophysiological studies of behaviour can provide insights into the proximate mechanisms of behaviour, but understanding the underlying evolutionary history can often reveal useful information that cannot be elucidated by studying molecular mechanisms alone. Therefore, in order to gain a full appreciation of behaviours in species interactions, ecological and evolutionary perspectives must be integrated. However, the ultimate causes of any neurophysiological phenomenon are understudied. In the context of parasites that alter host behaviour, considering the evolutionary history of the species interactions mainly involves analyzing whether an adaptive value exists (i.e., fitness advantage) for eliciting the specific behavioural changes in the host.

A central principle in evolutionary biology is that no beneficial trait can evolve without costs [1]. Therefore, the ability for a pathogen to manipulate host behaviour to its advantage must come at a price, such as forgoing further potential growth or fecundity [2]. The theory of adaptation by natural selection predicts that the fitness benefits should outweigh the costs of evolving the ability to manipulate host behaviour. Because ‘advantage’ in evolutionary terms is always relative, the adaptive hypothesis of behaviour manipulation is extremely difficult to test as the most recent non-manipulating ancestor is unlikely to be extant. Since directly testing the adaptive hypothesis often requires rare forms of evidence, such as fossil records, the best that we can do is to study the ecology of the extant species and then infer the evolutionary mechanisms. Alternatively, the behavioural changes in the host caused by the parasite are very useful in providing clues to the evolutionary mechanisms [3].

Intro Video: Just for Laughs
Here is a (very humorous) video that concisely summarizes the topic of this Wiki.
(Disclaimer: Some of the statements in this video may appear to prioritize hilarity over scientific literacy.)

Terminology

An important distinction must be made between adaptive and non-adaptive traits. Parasites may cause changes in host behaviour through one of two mutually exclusive mechanisms. First, the ability to cause behavioural change may arise through adaptation by natural selection. When a beneficial mutation occurs, natural selection will favour the persistence of that allele over the original, less advantageous alleles, eventually fixing it in the population. For instance, when a random mutation in a parasite allows it to elicit host response in such a way that facilitates the parasite’s transmission and thus increases its fitness, this new allele will be favoured and, given the right conditions, all individuals will inherit this allele within generations. This way of changing the host’s behaviour will be referred to as manipulation of host behaviour. Since most studies describe the ecology and behaviour of host-parasite interactions and lack direct testing of the adaptive hypothesis, the assertion that certain behaviours of the host benefit the parasite has been dubbed the manipulative hypothesis. The other type of changing host behaviour is not necessarily adaptive and results as a by-product of parasite infection (i.e., the behavioural change does not confer any fitness advantage to the parasite). Both types of mechanisms may be referred to as alteration of host behaviour, but will be more frequently used to refer to the behavioural changes that are hypothesized to be non-adaptive.

Furthermore, many parasites that alter host behaviour undergo complex lifecycles and require new hosts for each life stage. The definitive host is defined as the last host in the parasite’s lifecycle in which the parasite reproduces and dies. A parasite may have one or multiple intermediate hosts, which carry the parasite before it infects its definitive host [4].

Manipulation of Host Behaviour in the Wild

Figure 2
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An infected ant experiences tetanus of the mandibular muscles which
causes the ant to bite down on grass, waiting to be eaten by a grazing mammal.
Dicrocoelium dendriticum [Photograph]. (2009). Retrieved
March 28, 2013, from: http://en.citizendium.org/wiki/dicrocoelium_dendriticum

Ants go for a Hike: The Classic Dicrocoelium Mind Control

Figure 1
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D. dendriticum cyst in the subesophageal ganglion.
Arrows indicate mandibular nerves. (Adapted from [6].)

The lancet liver fluke, Dicrocoelium dendriticum, is commonly found in the liver and bile duct of grazing mammals such as sheep and cows and has a complex lifecycle, requiring several different hosts throughout ontogeny. They first infect terrestrial molluscs, such as snails, which leave behind slime trails that are ingested by ants, the second intermediate host.

Interestingly, behavioural changes observed in infected ants appear to enhance the parasite’s transmission to its definitive host, grazing mammals [5]. The parasite larvae infect the brain of the ants and encyst in the subesophageal ganglion (Figure 1) [6]. This area of infection is adjacent to the mandibular nerves, which explains the observed behavioural changes of the ants. The effects of behaviour manipulation are most apparent at night, when ants climb to the top of a blade of grass and bite down (Figure 2). The ants bite down on the grass because of the tetanus caused by the infection [5], and become immobile until dawn. This renders the ants very susceptible to accidental ingestion by grazing cattle or sheep, in which the D. dendriticum reproduces and completes its lifecycle.

Canopy Ants: Looking Berry Delicious

Figure 3
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Top: The resemblance of infected C. attratus ants to
berries commonly eaten by frugivorous birds.
Bottom: Infected ants constantly raise and flag their
red gasters. (Adapted from [7])

Even more complex than simply causing a host organism to exhibit abnormal behaviours is to manipulate the host to mimic other objects. Canopy ants sporting an unusual appearance were spotted by researchers and at first were mistaken to be a previously undiscovered species. Upon closer examination, these ants turned out to be the tropical canopy ants, Cephalotes atratus, infected with an unknown nematode species [7]. The infected ants displayed a wide array of morphological and behavioural changes. The normally black gaster (posteriormost portion of the abdomen) was bright red and filled with the parasite’s eggs (Figure 3) [7]. In addition, these ants were observed to constantly raise their red gaster in the air in a conspicuous manner [7], which may occur through the nerve damage caused by the parasite. As a result, these ants that live in trees end up resembling berries (Figure 3). When frugivorous birds mistake the infected ants for berries and ingest them, the nematode reaches the next stage in its lifecycle and reproduces in the bird.

Evidence of birds being this nematode’s definitive host comes from the observation that frugivorous bird feces in the studied region carried high densities of nematode eggs [7]. In turn, the worker adults of C. atratus colonies collect bird feces to feed the young and nematode larvae hatch and develop in the ant larvae. Furthermore, in a manipulative experiment, frugivorous birds attacked pink or red berry models more often than all of the other colours combined, suggesting that the induced redness of ant gasters indeed attracts these birds [7]. Therefore, this newly discovered nematode exemplifies a parasite that manipulates the behaviour of multiple hosts simultaneously through inducing mimicry. Further research of this phenomenon is required to understand the evolutionary history of the host-parasite interaction.

Caterpillar & Parasitoid Wasp: Conscripted by the Enemy's Army

Video 1. Violent head-swings
Host caterpillar guarding parasitoid pupae exhibits violent head-swings upon disturbance.

Background: Parasitoids

Parasitoids are organisms that parasitize other parasites. In ecology, parasitoids usually refer to small organisms that infect herbivores, and the herbivores are considered the ‘parasites’ of the plant. The presence of parasitoids is often beneficial to plants as they help to control the abundance of herbivore populations. Parasitoids are ubiquitous in nature and may account for a large proportion of global biodiversity. However, due to their inconspicuousness, parasitoid species richness is likely to be highly underestimated and the amount of research done on their biology remains disproportionately low.

Parasitoid wasps are a large clade within the order Hymenoptera. Each species of parasitoid wasp usually specializes on one herbivore host species. When an adult parasitoid infects a host, it lays eggs in the host’s body, and larvae subsequently hatch and develop. Parasitoids always kill their hosts eventually.

Glyptapanteles: The Ultimate 'Zombifier'

The parasitoid wasp, Glyptapanteles sp., does not manipulate host behaviour to increase its transmission to other hosts. Instead, Glyptapanteles tricks its host caterpillar, larva of the moth species Thyrinteina leucocerae, to become its guardian [8].

When the Glyptapanteles larvae developing inside of the host caterpillar are ready to pupate, they emerge from host’s body and encase themselves into cocoons near the host. At this point, the host is still alive but exhibits extremely bizarre behavioural changes [8]. First, the host stops feeding and moving. It remains very close to the pupae, and when it detects even a slight disturbance, it swings its head violently from side to side (Video 1). This motion is hypothesized to fend off predators that attempt to eat the gestating pupae [9]. Indeed, in a manipulative field experiment, the wasp pupae had a significantly higher survival in the presence of infected hosts than in their absence [8]. In addition to protecting its own parasites, the caterpillar spins silk on the pupae [8], which may help insulate the pupae or protect them further from predation. However, this is conjectural and requires further evidence. The host caterpillar dies once adult parasitoid wasps emerge from their cocoons.

Glyptapanteles is an extraordinary example of adaptive manipulation of host behaviour. This parasitoid wasp is especially unusual because it does not manipulate host behaviour for enhanced transmission, but does so to gain protection from predators. The proximate mechanisms by which the behavioural changes work remain yet to be elucidated by further research.

Grasshoppers & Hairworms: Involuntary Suicide

Figure 4
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An adult hairworm emerging from its host.
Spinochordodes tellinii [Photograph]. (2013). Retrieved
March 28, 2013, from: http://en.wikipedia.org/wiki/Spinochordodes_tellinii

The phylum Nematomorpha, commonly known as horsehair worms or hairworms, comprise exclusively of parasitoid worms. Nematomorphan larvae parasitize arthropod hosts in which they develop and then burst out as freeliving adults, killing the host (Figure 4). The hosts of nematomorphans are often members of order Orthoptera, which includes grasshoppers, katydids, and crickets. One nematomorphan, Spinochordodes tellinii, has been found to elicit abnormal behaviours in a grasshopper species, Meconema thalassinum, upon infection. The infected grasshopper seeks a body of water and then jumps into it, at which time the developed S. tellinii adults emerge and mate in the water [10]. The parasitoid not only induces this change in host behaviour, but also times it precisely such that the ‘suicide jump’ occurs only at night [11].

Studies that investigate the proximate mechanisms underlying ethological phenomena are rare. However, one study examined the differential protein expression that occurs in both the parasitoid and the host during infection [11]. The authors of this study used a proteomics approach (see Physiological Mechanisms of Parasitic Alteration of Host Behaviour: Proteomics), rather than studying specific gene targets that are selected a priori, allowing for an unbiased assay of all gene products [12]. Within the grasshopper’s central nervous system (CNS), six protein families involved in the proper development of the CNS were expressed, indicating that there was a host response to protect against parasitic CNS invasion [11]. In addition, a protein involved in spatial navigation was expressed in the host, which explained the grasshopper’s tendency to seek water bodies [11].

Furthermore, the parasitoid itself was shown to release proteins inside the host to influence the host CNS. These were proteins involved in the regulation of apoptosis or neurotransmitter release [11]. Indeed, among parasite manipulation systems, apoptosis of host neurons is a common mechanism used to elicit certain behaviours in hosts [13]. In this host-parasite system, the changes in host behaviour are mediated by both the chemical manipulation of the parasitoid and the endogenous host response to infection.

Parasites that Alter Human Behaviour

Video 2. Toxoplasmosis in Rodent
The silencing effects of T. gondii infection on rodent's anti-predatory behaviour.

Currently, there are no known parasites that manipulate human behaviour to their advantage. An anecdotal report of malarial infections making humans smell more attractive to mosquito vectors exists, but this remains an untested hypothesis. Many parasites that manipulate other mammal hosts, however, do alter human behaviour as well, since humans and other mammals share much of the neurophysiological processes in common. The result is changes in human behaviour as a by-product of parasite infection, which appear to confer the parasite no fitness benefits. Therefore, humans are often accidentally infected secondary hosts and are ‘dead-ends’ in the lifecycle of the parasites. We may speculate that manipulation of human behaviour did not evolve because humans are not subject to predation by other species, and thus cannot serve as intermediate hosts to parasites with complex lifecycles. Here, three parasitic diseases that inflict humans are discussed: toxoplasmosis, rabies, and trypanosomiasis. In addition, the host-parasite relationships between those parasites and their natural hosts are described.

Toxoplasmosis

Ecology of Toxoplasma gondii

The protozoan intracellular parasite, Toxoplasma gondii, can affect a wide range of mammal hosts. Like many hosts that alter host behaviour, T. gondii requires multiple hosts throughout ontogeny to complete its lifecycle. The behaviours elicited in rodents are thought to be advantageous for the parasite’s transmission to the definitive feline host [14,15]. Infected rodents display decreased fear responses to novel objects, increased exploratory behaviour [16,17], and reduced vigilance for predators (Video 2) [18]. They also exhibit increased overall activity [14], which makes them more conspicuous to predators.

Lifecycle of Toxoplasma gondii

The intracellular parasite Toxoplasma gondii undergoes a complex lifecycle consisting of three main stages: the tachyzoite, which invades the host cell and multiplies; the bradyzoite, which forms cysts within the host CNS; and finally the sporozoite, which is found in oocysts and is highly tolerant to environmental stressors (Figure 5) [19]. Members of the family Felidae (cats) are the definitive hosts of T. gondii, and oocysts are released through their feces. Oocysts are encapsulated zygotes of the protozoan which are inhaled or ingested by a rodent, the parasite’s first host.

Figure 5
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The lifecycle of T. gondii (adapted from [19]).

Human Toxoplasmosis

Toxoplasmosis affects one third of the global human population [20]. Many organs of the body are affected, but the invasion of the central nervous system (CNS) is what leads to the observed behavioural changes. Congenital toxoplasmosis occurs when pregnant women become infected with T. gondii, which can occur by various routes of transmission, including eating undercooked meat and handling cat litter. The tachyzoite is the life stage that infects pregnant women and their fetuses. Symptoms of congenital toxoplasmosis may not appear until 20 to 30 years of age and can include seizures, mental retardation, deafness, blindness, intracranial calcifications, and death [19].

Postnatal toxoplasmosis infections manifest in a wide array of neural symptoms. A correlational study found that individuals that attempted suicide had significantly higher levels of IgG antibodies to T. gondii than individuals who did not attempt suicide [21]. Psychomotor function was compromised in infected patients, and they were shown to be at a 2.6-fold higher risk of car accidents [22].

Although cats are the definitive hosts for T. gondii, humans can accidentally become infected as a secondary host. Because humans are not intermediate hosts for T. gondii, infected humans do not exhibit behaviours that appear to serve the parasite. However, many behavioural changes result as by-products of parasite infection in the CNS. Although humans are currently not subject to feline predation, this was not the case for our primate ancestors. Therefore, some of the behaviours exhibited by T. gondii-infected rodents may be similar to behavioural changes in humans, and many neurophysiological studies use rodent models to understand the effects of toxoplasmosis in humans.

Toxoplasmosis and Schizophrenia

Also see Schizophrenia.

A growing body of evidence links toxoplasmosis to schizophrenia. Individuals afflicted with schizophrenia show increased levels of antibodies to T. gondii than healthy individuals [23]. Also, congenital toxoplasmosis has been linked to the development of schizophrenia [24]. Not only are there associations between elevated levels of T. gondii antibodies and the incidence of schizophrenia, but evidence also points to the antibody increase preceding the onset of schizophrenia, reaching maximum antibody levels approximately six months before onset [25]. This suggests that Toxoplasma infections may induce the expression of schizophrenia in individuals. The toxoplasmosis hypothesis of schizophrenia is further supported by the finding that cat ownership is associated with a higher incidence of schizophrenia than expected by chance [26]. Human contact with cat feces is one of the main routes of T. gondii transmission.

Moreover, drug treatment for schizophrenia has shown to decrease antibody levels to T. gondii [27]. Also, the tachyzoite form of T. gondii exhibited slowed growth in vitro in response to antipsychotic drug treatments [28]. These results indicate that antipsychotic drugs may reduce the positive symptoms of schizophrenia through suppressing T. gondii growth and replication. Indeed, T. gondii-infected rats treated with antipsychotic drugs were shown to no longer exhibit the ‘suicidal’ passivity to feline predation [29]. The mechanism by which antipsychotic drugs act on T. gondii is likely to work by interfering with the functions of calcium by blocking calcium channels or calmodulin activity, as tachyzoites need calcium to invade host cells [30]. Other effects of T. gondii infections involve neuromodulatory systems. Infections were found to be associated with elevated dopamine levels [31], which is consistent with the increased incidence of schizophrenia.

Neuropathology of Toxoplasmosis

Figure 6
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Microscopy of a mouse brain section shows a neuron containing
multiple bradyzoite cysts (adapted from [15]).

Also see Physiological Mechanisms of Parasitic Alteration for in-depth neurophysiology of toxoplasmosis.

Different strains of Toxoplasma gondii exhibit varying degrees of migratory ability within the host body [32]. Tachyzoites, upon invasion of the human body, exploit migratory dendritic cells and macrophages to invade the CNS, where they encyst and differentiate into bradyzoites (Figure 6) [32]. Subsequently, symptoms of toxoplasmosis manifest in behavioural changes as both direct and indirect effects. Immune responses can mediate indirect effects to change the host behaviour, whereas direct effects arise from alteration of neural pathways [15]. Some of the mechanisms of direct effects are discussed here.

One prevalent outcome of T. gondii infection in the brain is neurodegeneration. However, neurodegeneration does not occur globally throughout the CNS, as cyst formation occurs in specific locations of the brain. Thus, behaviours governed by unaffected brain regions are not altered in T. gondii-infected rodents, such as social and mating behaviours [14]. Cysts were found to localize in specific brain structures, including amygdala, nucleus accumbens [33], olfactory bulb [34], cortex, cerebellum, basal ganglia, perihippocampal areas, and medulla [15].

The effect of Toxoplasma infection on the olfactory system is to increase rodent vulnerability to cat predation by inactivating cat-specific odour receptors [15]. The limbic system is also affected by T. gondii, and the main outcome of this in the rodent host is a diminished level of anxiety toward novel objects and predators. The anxiolytic effects of toxoplasmosis were confirmed by a study which showed that rats inoculated with higher concentrations of T. gondii explored the elevated-plus maze to a greater extent, indicating reduced anxiety [33].

Another way in which T. gondii induces major behavioural changes is through tampering with normal neuromodulatory pathways. The most significant change observed is the chronic elevation of dopamine levels, which has also been consistently linked to schizophrenia in humans. High dopaminergic activity is further implicated in the increased overall activity in rodents due to the hyperactive nigrostriatal pathway [17]. Dopamine also affects mesolimbic structures and the prefrontal cortex and is thought to enhance exploratory tendencies [35]. Interestingly, the parasite may itself contribute to elevated dopamine levels in the host by producing its own L-DOPA, the precursor molecule of dopamine [36].

Rabies

Video 3. Rabies in a Human Patient
The progression of rabies in a human patient.

Rabies is a deadly viral infection that inflicts a wide range of hosts and is often transmitted through biting. Today, rabies remains a serious infectious disease in developing countries [37]. The rabies virus does not have a complex lifecycle, so it simply gains a fitness advantage from widespread transmission. The increased aggression in infected animals aids this process through salivary transmission. The manipulation hypothesis is further supported by the fact that the rabies virus affects phylogenetically conserved brain structures, which allows the pathogen to infect a high diversity of host species.

Neuropathology of Rabies

In mammals, the rabies virus invades the CNS and causes neuronal apoptosis in the hippocampus, amygdala, and hypothalamus [38]. Apoptosis induction is a common mechanism by which parasites alter host behaviour [13]. Neurotransmitter release and neuromodulatory systems are also affected by rabies infection. In particular, serotonin release [39] and binding [40] are significantly reduced. Also, opioid receptor binding [41] and GABA transmission are reduced [42]. Aggression, the signature behavioural change of rabies, is likely mediated through the change in serotonin activity. In fact, the adjective ‘rabid’ is derived from the behaviour exhibited by rabies-infected animals. As a consequence of heightened aggression, rabies-infected animals also exhibit increased rates of biting, which ultimately enhance transmission of the virus.

Video 4. Hydrophobia
Suspected rabies patient in Vietnam exhibits hydrophobia.

Upon entering the muscle of a bitten animal, the virus transduces into the CNS via a neuromuscular junction [43,44]. First, the characteristic glycoprotein expressed by the virus mediates invasion into a peripheral neuron near the infected muscle cell through the interaction with various neuron surface molecules, including nicotinic acetylcholine receptors and the neural cell adhesion molecule (NCAM) [45]. The virus then invades the CNS by retrograde axonal transport [43], then replicates and causes the cellular and chemical changes described above.

Rabies in Humans

Humans can become infected with rabies virus if bitten by a rabid animal. As in other animals, humans invariably die very shortly after infection, normally within a few days. Key clinical symptoms of rabies include restlessness, hydrophobia, and aerophobia (Video 3; Video 4). Rabies patients exhibit a fear of drinking water and receiving air puffs to the face because both trigger painful muscular contractions in the larynx and pharynx [46]. Other symptoms result from the deterioration of autonomic function, such as uncontrolled perspiration, salivation, and pupil dilation [47]. During the final stages of the infection, rabies patients experience paralysis of the limbs and cardiac arrhythmia. Ultimately, they fall into a coma and die. Rabies is untreatable but is preventable with a vaccine.

Trypanosomiasis

Figure 7
Image Unavailable
Lifecycle of Trypanosoma.
Trypanosoma [Photograph]. (2010). Retrieved March 31, 2013,
from: http://microbewiki.kenyon.edu/index.php/Trypanosoma

Trypanosomiasis, commonly known the sleeping sickness, is caused by an extracellular protozoan parasite of the genus Trypanosoma. Several variations of the disease exist, depending on the species and strain of the infecting Trypanosoma. Two main categories of the disease are the African sleeping sickness, which is caused by Trypanosoma brucei, and the Chagas disease (also American sleeping sickness) caused by T. cruzi. Like other common infectious diseases such as malaria, Trypanosoma is transmitted among mammals through a blood-sucking vector, the tsetse fly (Glossina sp.) (Figure 7).

Trypanosomiasis is divided into two clinical stages. The first stage is the haemolymphatic stage, during which the parasite develops in the blood and lymph nodes. In the late encephalitic stage, the parasite invades the CNS by altering the blood-brain barrier [48]. The cerebrospinal fluid of African trypanosomiasis patients was shown to induce apoptosis in endothelial cells and microglial cells, in vitro [49]. Both of these cell types are important components of blood-brain barrier structure and function (see Immunology of Alzheimer's Disease). As we have observed for various host-parasite interactions, apoptosis is a common mechanism of pathogenesis and behaviour alteration (see Grasshoppers & Hairworms: Involuntary Suicide, Toxoplasmosis, and Rabies).

The most common clinical symptoms of trypanosomiasis are sleeping disorders, headaches, and lymphadenopathy [50]. Trypanosoma infection results in disturbances in the host’s circadian rhythm. Infected rats exhibit a decreased overall level of melatonin secretion as well as a temporal shift in the maximal melatonin receptor binding at the suprachiasmatic nucleus of anterior hypothalamus, in comparison to uninfected rats [51]. Humans infected with Trypanosoma likely also experience sleeping disorders due to this abnormal activity of melatonin. Another outcome of trypanosomiasis is chronic depressive-like behaviour. In a mouse model, serotonin selective reuptake inhibitors (SSRIs) and anti-parasite drugs were shown to reduce the symptoms of depression [52], indicating that Trypanosoma was the causative agent of depressive behaviours. Other neurological symptoms, such as disturbance in appetite and speech functions, overall reduced activity, tremor, and other signs of the broadly categorized ‘unusual behaviours’ are variably expressed [50].

Evolutionarily advantageous aspects of the behavioural changes in hosts induced by Trypanosoma are still unclear. One possibility is that the behavioural changes are simply by-products of infection, rather than a manipulation evolved to serve the parasite. Alternatively, we can speculate that decreased overall activity may facilitate easier contact with the vector flies, and thus more efficient spread of the disease. Indeed, the densities of hosts and vectors significantly affect the transmission of Trypanosoma [53]. Further research of the ecology and neuropathological mechanisms of trypanosomiasis is warranted.

Acknowledgements

This Wiki was entirely written and edited by Rufina Kim. I would like to thank Jessica Li and Abir Arefin for contributing to the main group page, Parasites That Alter Host Behaviour, as well as the authors of the numerous Wiki pages which I have hyperlinked throughout this page. Lastly, I would like to thank Professor Ju for providing me technical comments and encouragement to pursue this project.

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