Parasites That Alter Host Behaviour

Host-parasite relationships are ubiquitous throughout nature, but of curious interest are those parasites that induce behavioural changes in the host. Studies of this phenomenon began to emerge in the 1950s, beginning with the ethological analysis of the great cormorant (Phalacorcorax carbo), in which fish eaten by these birds were found to have a higher rate of infection by a cestode worm parasite.[1] The great cormorants are the definitive host in the lifecycle of the parasite species and the infected fish, intermediate hosts for the cestode, somehow behaved differently as to be more susceptible to predation by the great cormorants.[1] A theory that attempted to explain such observations in an evolutionary ecology perspective was popularized, and was called the manipulation hypothesis. This hypothesis took an adaptationist view and contended that some parasites evolved through natural selection the ability to alter their host’s behaviour in order to complete their lifecycle, in addition to increasing their transmission rate.[1] Furthermore, humans are also susceptible to parasites that invade the central nervous system. However, humans appear less likely to be victims of behaviour manipulation, per se, as humans are not intermediate hosts to any known parasite. Nonetheless, many of these parasites have serious consequences on the human nervous system as byproduct of their infection mechanism and metabolism. For instance, a tapeworm (Taenia solium) infection, often ingested in undercooked pork, causes neurocysticercosis.[2] Another common human parasite is Toxoplasma gondii, which induces personality changes and reduced reaction times in humans.[3] Parasitic diseases affect vast numbers of humans worldwide, and thus studying the neurophysiology and ecology of highly transmissible parasites is of paramount importance for prevention and treatment.

Bibliography
1. Thomas F, Moore J, Poulin R, Adamo S. (2007). Parasites that Manipulate Their Hosts. In Encyclopedia of Infectious Diseases. (pp. 299-313). Hoboken, New Jersey: John Wiley & Sons.
2. Zimmer C. (2012, June). Hidden Epidemic: Tapeworms Living Inside People’s Brains. Discover Magazine. Retrieved from http://discovermagazine.com/2012/jun/03-hidden-epidemic-tapeworms-in-the-brain#.USmaYqVJP4t.
3. Webster JP, McConkey GA. Toxoplasma gondii-altered host behaviour: clues as to mechanism of action. Folia Parasitologica. (2010) 57(2):95-104


Methods and Techniques for Studying Parasite-Induced Neurological Changes

main article: Methods and Techniques for Studying Parasite-Induced Neurological Changes
author: Abir Arefin

Neurocysticercosis
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Networks of tapeworms colonizing in the fluid-filled cavities of the brain.
Taenia solium cysts [Photograph]. (2012). Retrieved March 1, 2013, from:
http://discovermagazine.com/2012/jun/03-hidden-epidemic-tapeworms-in-the-brain.

In the past, the popular theory explaining why parasites alter their host’s behaviour was the manipulation hypothesis. This theory states that parasites altered their host’s behaviour in order to increase their transmission rate and thereby increase their own selective benefit[1]. There is a great multitude of case studies that would support this theory; however, recent studies using brain imaging technologies have revealed a new possibility. Changes made to the brain by parasitic infections may be a result of the host’s physiological response to the infection[2], as in the case of neurocysticercosis, a condition where brain tapeworms create lesions in the human brain[5]. In this section, various popular methods used to study the effects of parasites on the host’s brain will be discussed. The most common method used to study the effects of parasites on host neurological function is magnetic resonance imaging (MRI)[3]. A major limitation with the MRI method is that it fails to confirm whether the image results are illustrative of parasitic alterations for their own adaptive benefit or whether the damage is merely due to the host’s immune responses[3]. Therefore, the existing controversy in this field is ongoing and scientists are searching for methods that will display more definitive findings. They must account for instances in which the manipulation hypothesis does not ring true through correlation studies [4].

Bibliography
1. Thomas F, Moore J, Poulin R, & Adamo S. (2007). Parasites that Manipulate Their Hosts. In Encyclopedia of Infectious Diseases. (pp. 299-313). Hoboken, New Jersey: John Wiley & Sons.
2. Tain L, Perrot-Minnot M, & Cezilly F. Altered host behaviour and brain serotinergic activity caused by acanthocephalans: evidence for specificity. Proceedings of the Royal Society. (2006) 273(1605): 3039-3045.
3. Khan A. (2011, May). Imaging in CNS Toxoplasmosis. Medscape Reference. Retrieved from http://emedicine.medscape.com/article/344706-overview.
4. Hermes G, Ajioka J, Kelly K, Mui E, Roberts F, et al. Neurological and behavioural abnormalities, ventricular dilation, altered cellular functions, inflammation, and neuronal injury in brains of mice due to common, persistent, parasitic infection. Journal of Neuroinflammation. (2008) 5: 48.
5. Lucato LT, Guedes MS, Sato JR, Bacheschi LA, Machado LR, et al. The role of conventional MR imaging sequences in the evaluation of neurocysticercosis: impact on characterization of the scolex and lesion burden. American Journal of Neuroradiology. (2007) 28: 1501-1504.


Neuroethology of Parasites That Alter Host Behaviour

main article: Neuroethology of Parasites That Alter Host Behaviour
author: Rufina K

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.)
Bibliography
1. Frank SA. Models of parasite virulence. The Quarterly Review of Biology. (1996) 71(1): 37-78.
2. Poulin R. The evolution of parasite manipulation of host behavior: a theoretical analysis. Animal Behaviour. (1994) 109:S109-S118.
3. Thomas F, Adamo S, Moore J. Parasitic manipulation: where are we and where should we go? Behavioural Processes. (2005) 68:185-199.


Physiological Mechanisms of Parasitic Alteration of Host Behaviour

main article: Physiological Mechanisms of Parasitic Alteration of Host Behaviour
author: JessLi

Gypsy moth larvae
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In the late stages of LdMNPV infection,
gypsy moth larvae climb to treetops and die.
Retrieved from [http://www.nature.com/news/2011/110908/full/news.2011.526.html]

Although a great diversity of parasite-induced changes in host behaviour has been documented, the physiological mechanisms utilized by these parasites are not well known. Current research has looked primarily at parasite-induced changes to biogenic amine systems. In many animals, biogenic amine systems control a variety of functions including locomotion, feeding, predator avoidance behaviours, and motivation. It is difficult to clearly define pathways and mechanisms of parasitic manipulation in these systems due to the complex range of behaviours affected by even a single transmitter[1]. Nonetheless, changed levels of neurotransmitters such as serotonin, dopamine, and octopamine (an invertebrate neuromodulator) are correlated with abnormal behaviour in infected animals[2]. In addition to modifying biogenic amine systems, some parasites target specific areas and circuitry of their host organism’s central nervous system to affect a particular behaviour[3]. Finally, some studies are using modern genetic and proteomic techniques to look at the way parasites may cause changes through altering their hosts' proteomic profiles[4].

Bibliography
1. Perrot-Minnot, M.-J. & Cézilly, F. Investigating candidate neuromodulatory systems underlying parasitic manipulation: concepts, limitations and prospects. The Journal of Experimental Biology 216, 134-141 (2013).
2. Adama, S.A. Parasites: evolution's neurobiologists. The Journal of Experimental Biology 216, 3-10 (2013).
3. Gal, R. & Libersat, F. A wasp manipulates neuronal activity in the sub-esophageal ganglion to decrease the drive for walking in its cockroach prey. PLoS One 4, 1-10 (2010).
4. Hoover, K et al., A gene for an extended phenotype. Science 333,1401 (2011).



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