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Behavior-altering parasite

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Some parasites and parasitoids cause changes in the behavior of their hosts by directly affecting the hosts' decision-making and behavior control mechanisms. The acquired or modified behaviors assist in parasite transmission, and often result in the host's demise.

Types of behavioral change

Parasites may alter hosts' behaviors in ways that enhance the likelihood of parasite transmission from host to host (eg. by host predation); result in parasite release at appropriate sites (eg. by changes in the host's preferences for habitat selection); increase parasite survival[1] or increase the host’s likelihood of colonization by suitable mates for the parasite.

The protozoan Toxoplasma gondii infects animals from the Felidae family (its definitive host), and its oocysts are shed with the host's feces. When a rodent consumes the fecal matter it gets infected with the parasite (becoming its intermediate host). The rodent subsequently becomes more extroverted and less fearful of felines, increasing its chance of predation and the parasite's chance of completing its lifecycle. There is some evidence that T. gondii, when infecting humans, alters their behavior in similar ways to rodents; it has also been linked to cases of schizophrenia.[2] Other parasites that increase their host's risk of predation include Euhaplorchis californiensis, Dicrocoelium dendriticum and Myrmeconema neotropicum.

Plasmodium falciparum, carried by the Anopheles gambiae mosquito, changes its host's attraction to sources of nectar in order to increase its sugar intake and enhance the parasite's chance of survival.[3]

The Emerald cockroach wasp (Ampulex compressa) parasitises its host, the American cockroach (Periplaneta americana) as a food source and for its growing larvae. Unlike other parasites, the wasp induces the behavioral change prior to infecting the host, putting it into a state of hypokinesia - "a reversible long-term lethargy characterized by lack of spontaneous movement or response to external stimuli".[4] The cockroach remains alive but motionless, and after dragging it to a burrow the wasp deposits an egg into its carcass and buries it for the growing larva to feed on. The adult wasp emerges after 6 weeks, leaving behind nothing but a hard outer cockroach "shell".[4]

The parasitic wasp Hymenoepimecis argyraphaga grows its larvae on spiders of the species Leucauge argyra. Shortly before killing its host the larva induces changes in the spider's weaving behavior, causing it to weave a strong, cocoon-like structure. The larva then kills, enters the cocoon and pupates.[5]

Strepsiptera of the Myrmecolacidae family can cause their ant host to linger on the tips of grass leaves, increasing the chance of being found by the parasite's males (in case of females) and putting them in a good position for male emergence (in case of males).[6] A similar, but much more intricate behavior is exhibited by ants infected with the fungus Ophiocordyceps unilateralis: irregularly-timed body convulsions cause the ant to drop to the forest floor,[7] from which it climbs a plant up to a certain height[8] before locking its jaws into the vein of one of its leaves answering a certain criteria of direction, temperature and humidity. After several days the fruiting body of the fungus grows from the ant's head and ruptures, releasing the fungus's spores.[9]

Evolutionary perspective

The adaptive manipulation hypothesis posits that specific behavioral alterations induced in a host can be used by parasites to increase their fitness. Under this hypothesis, induced behaviors are the result of natural selection acting upon the parasite’s extended phenotype (in this case its host's behavior). Many behaviors induced by obligate parasites to complete their lifecycles are examples of adaptive manipulation because of their clear relationship to parasite fitness. For example, evidence has shown that infection by the parasitic worm Pomphorhynchus laevis leads to altered drifting behavior in its intermediate host, the amphipod Gammarus pulex. This altered behavior increases its host's predation risk by fish which are P. laevis’s definitive hosts. The induced behavioral change in the host thus leads to the parasite’s increased success in completing its life cycle.[10]

Mechanisms

The way in which parasites induce behavioral changes in hosts has been compared to the way a neurobiologist would affect a similar change in a lab.[11] A scientist may stimulate a certain pathway in order to produce a specific behavior, such as increased appetite or lowered anxiety; parasites also produce specific behavioral changes in their hosts, but rather than stimulate specific neurological pathways, they appear to target broader areas of the central nervous system. While the proximate mechanisms underlying this broad targeting have not been fully characterized, two mechanisms used by parasites to alter behavior in vertebrate hosts have been identified: infection of the central nervous system and altered neurochemical communication.[12]

Infection of the central nervous system

Some parasites alter host behavior by infecting neurons in the host’s central nervous system. The host’s central nervous system responds to the parasite as it would to any other infection. The hallmarks of such response include local inflammation and the release of chemicals such as cytokine. The immune response itself is responsible for induced behavioral changes in many cases of parasitic infection. Parasites that are known to induce behavioral changes through central nervous system inflammation in their hosts include Toxoplasma gondii'' in rats, Trypanosoma cruzi in mice and Plasmodium mexicanum in the Mexican lizard.[12]

Toxoplasma gondii induces behavioral changes in rats by infecting neurons in the central nervous system.

While some parasites exploit their hosts’ typical immune responses, others seem to alter the immune response itself. For example, the typical immune response in rodents is characterized by heightened anxiety.[13] Infection with Toxoplasma gondii inhibits this response, increasing the risk of predation by T. gondii’s subsequent hosts. Research suggests that the inhibited anxiety-response could be the result of immunological damage to the limbic system.[11]

Altered Neurochemical Communication

Parasites that induce behavioral changes in their hosts often exploit the regulation of social behavior in the brain.[12] Social behavior is regulated by hormones, such as dopamine and serotonin, in the emotional centers of the brain - primarily the amygdala and the hypothalamus, and although parasites may be capable of stimulating specific neurochemical pathways to induce behavioral changes, evidence suggests that they alter neurochemical communication through broad rather than specific targeting.[11] For example, Toxoplasma gondii attaches to the hypothalamus rather than target a specific cellular pathway; this broad targeting leads to a widespread increase in host dopamine levels, which may in turn account for the loss of aversion to cat odor.[14] In some cases, T. gondii is believed to cause increases in dopamine levels by secreting another compound, L-Dopa, which may trigger a rise in dopamine levels, though concrete evidence for this mechanism has not yet been demonstrated.[14] This rise in dopamine levels induces a loss of aversion to cat odor in the rats, increasing the risk of predation by cats, T. gondii’s definitive host.[14] The mechanistic details underlying the increase in dopamine levels and the way it affects the rat's behavioral change remain elusive.[11]

The emerald cockroach wasp alters behavior through the injection of venom directly into the host’s brain, causing hypokinesia.[12] While the host's brain circuitry responsible for control of movement is still functional, the nervous system is in depressed state. Movement in the host is controlled by dopamine and octopamine which affect transmission of interneurons involved in the natural response to escape, and the reduced motor activity results from a reduction of these amines.[4]

The original function of such secretions may have been to suppress the immune system of the host (see above). The trematode Schistosoma mansoni secretes opioid peptides into the host's bloodstream, influencing both its immune response and neural function.[15] Other sources suggest a possible source in molecular mimicry.[16]

Other mechanisms

Both hairworms and mermithid nematodes induce water-seeking behavior in their respective hosts,[1][17] but while the former manipulates its host's brain chemistry,[18] the latter relies on altering the host's hemolymph osmolality (concentration of salt) to achieve the same effect.[17]

References

  1. ^ a b Thomas, F.; Schmidt-Rhaesa, A.; Martin, G.; Manu, C.; Durand, P.; Renaud, F. (May 2002). "Do hairworms (Nematomorpha) manipulate the water seeking behaviour of their terrestrial hosts?" (PDF). J. Evol. Biol. 15 (3): 356–361. doi:10.1046/j.1420-9101.2002.00410.x.
  2. ^ "Higher Extraversion and Lower Conscientiousness in Humans Infected with Toxoplasma - Lindová - 2011 - European Journal of Personality - Wiley Online Library". Retrieved 2015-09-17.
  3. ^ V.O., Nyasembe; et al. (2014). "Plasmodium falciparum Infection Increases Anopheles gambiae Attraction to Nectar Sources and Sugar Uptake". Current Biology. 24: 1-5. doi:10.1016/j.cub.2013.12.022. PMID 24412210.
  4. ^ a b c Banks, Christopher N.; Michael E. Adams (2012). "Biogenic amines in the nervous system of the cockroach, Periplaneta americana following envenomation by the jewel wasp, Ampulex compressa". Toxicon. 59 (2): 320–328. doi:10.1016/j.toxicon.2011.10.011. ISSN 0041-0101. Retrieved 2013-02-22..
  5. ^ W.G, Ebenhard (2000). "Spider manipulation by a wasp larva" (PDF). Nature. 406: 255–256.
  6. ^ Wojcik, Daniel P. (1989). "Behavioral Interactions between Ants and Their Parasites". The Florida Entomologist. 72 (1): 43–51. doi:10.2307/3494966. ISSN 0015-4040. JSTOR 3494966.
  7. ^ Hughes DP, Andersen SB, Hywel-Jones NL, Himaman W, Billen J, Boomsma JJ (May 2011). "Behavioral mechanisms and morphological symptoms of zombie ants dying from fungal infection". BMC Ecology. 11 (1): 13–22. doi:10.1186/1472-6785-11-13. PMC 3118224. PMID 21554670.{{cite journal}}: CS1 maint: unflagged free DOI (link)
  8. ^ Andersen SB, Gerritsma S, Yusah KM, Mayntz D, Hywel-Jones NL, Billen J, Boomsma JJ, Hughes DP (September 2009). "The life of a dead ant: The expression of an adaptive extended phenotype". The American Naturalist. 174 (3): 424–433. doi:10.1086/603640. JSTOR 10.1086/603640. PMID 19627240.
  9. ^ Sample, Ian (18 August 2010). "'Zombie ants' controlled by parasitic fungus for 48m years". News » Science » Microbiology. The Guardian. Retrieved 2010-08-22.
  10. ^ Lagrue, Clément; Kaldonski, Nicolas; Perrot-Minnot, Marie J.; Motreuil, Sébastien; Bollache, Loïc (Nov 2007). "Modification of hosts' behavior by a parasite: field evidence for adaptive manipulation". Ecology. 88 (11): 2839–2847. doi:10.1890/06-2105.1. ISSN 0012-9658. PMID 18051653.
  11. ^ a b c d Thomas, edited by David P. Hughes, Jacques Brodeur, Frédéric; Brodeur, J; Thomas, F (2012). Host manipulation by parasites. Oxford: Oxford University Press. ISBN 978-0-19-964224-3. {{cite book}}: |first1= has generic name (help)CS1 maint: multiple names: authors list (link)
  12. ^ a b c d Klein, Sabra L. (Aug 2003). "Parasite manipulation of the proximate mechanisms that mediate social behavior in vertebrates". Physiology & Behavior. 79 (3): 441–449. doi:10.1016/s0031-9384(03)00163-x. ISSN 0031-9384. PMID 12954438.
  13. ^ Lacosta, S.; Merali, Z.; Anisman, H. (1999-02-13). "Behavioral and neurochemical consequences of lipopolysaccharide in mice: anxiogenic-like effects". Brain Research. 818 (2): 291–303. doi:10.1016/s0006-8993(98)01288-8. ISSN 0006-8993. PMID 10082815.
  14. ^ a b c Webster, J. P. (Dec 1994). "The effect of Toxoplasma gondii and other parasites on activity levels in wild and hybrid Rattus norvegicus". Parasitology. 109 (5): 583–589. doi:10.1017/s0031182000076460. ISSN 0031-1820. PMID 7831094.
  15. ^ M., Kavaliers; et al. (1999). "Parasites and behavior: an ethopharmacological analysis and biomedical implications" (PDF). Neuroscience and Biobehavioral Reviews. 23: 1037–1045. doi:10.1016/s0149-7634(99)00035-4.
  16. ^ Biron, D. G.; et al. (2005). "Behavioural manipulation in a grasshopper harbouring hairworm: a proteomics approach" (PDF). Proceedings of the Royal Society B. 272 (1577): 2117–21126. doi:10.1098/rspb.2005.3213. PMC 1559948. PMID 16191624.
  17. ^ a b C.M., Williams (2004). "Increased haemolymph osmolality suggests a new route for behavioural manipulation of Talorchestia quoyana (Amphipoda: Talitridae) by its mermithid parasite". Functional Ecology. 18: 685–691. doi:10.1111/j.0269-8463.2004.00910.x.
  18. ^ Thomas, F.; et al. (2003). "Biochemical and histological changes in the brain of the cricket Nemobius sylvestris infected by a manipulative parasite Paragordius tricuspudatus (Nematomorpha)". International Journal for Parasitology. 33 (4): 435–443. doi:10.1016/S0020-7519(03)00014-6.
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