Behavior-altering parasites are parasites capable of causing changes in the behavior of their hosts species to enhance their transmission, sometimes directly affecting the hosts' decision-making and behavior control mechanisms. By way of example, a parasite that reproduces in an intermediate host may require, as part of their life cycle, that the intermediate host be eaten by a predator at a higher trophic level, and some parasites are capable of altering the behavior of the intermediate host to make such predation more likely; a mechanism that has been called parasite increased trophic facilitation or parasite increased trophic transmission. Examples can be found in bacteria, protozoa, viruses, and animals. Parasites may perform bodyguard manipulation to increase protection of the parasites or their offspring.
Among the behavioral changes caused by parasites is carelessness, making their hosts easier prey. The protozoan Toxoplasma gondii, for example, infects small rodents and causes them to become careless and may cause them to become attracted to the smell of cat urine, both of which increase their risk of predation and the parasite's chance of infecting a cat, its definitive host.
Parasites may alter the host's behavior by infecting the host's central nervous system, or by altering its neurochemical communication (studied in neuroparasitology).
Mechanisms
Direct and indirect manipulation
Parasite manipulations can be either direct or indirect. Indirect manipulation is the most frequent method used by behavior-altering parasites, while the direct approach is far less common. Direct manipulation is when the parasite itself affects the host and induces a behavioral response, for example by creating neuroactive compounds that stimulate a response in the host's central nervous system (CNS), a method mostly practiced by parasites that reside within the CNS. Affecting the host's neural system is complicated and manipulation includes initiating immune cascades in the host. However, determination of the causative factor is difficult, especially whether the behavioral change is the result of direct manipulation from the parasite, or an indirect response of the host's immune system. A direct approach to behavioral manipulation is often very costly for the parasite, which results in a trade-off between the benefits of the manipulation (e.g., fitness increase) and the energy it costs. The more common approach for parasites is to indirectly induce behavioral responses by interacting with the host's immune system to create the necessary neuroactive compounds to induce a desired behavioral response. Parasites can also indirectly affect the behavior of their hosts by disturbing their metabolism, development, or immunity. Parasitic castrators drastically modify their hosts' metabolism and reproduction, sometimes by secreting castrating hormones, changing their behavior and physiology to benefit the parasite.
The ways in which parasites induce behavioral changes in hosts have been compared to the way a neurobiologist would effect a similar change in a lab. 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.
Central nervous system infection
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 cytokines. 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.
Immune response
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. Infection with Toxoplasma gondii inhibits this response, increasing the risk of predation by T. gondiis subsequent hosts. The inhibited anxiety-response could be the result of immunological damage to the limbic system.
Altered neurotransmission
Parasites that induce behavioral changes in their hosts often exploit the regulation of social behavior in the brain. Social behavior is regulated by neurotransmitters, 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. 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. 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. This rise in dopamine levels induces a loss of aversion to cat odor in the rats, increasing the risk of predation by cats, T. gondiis definitive host. The mechanism of the increase in dopamine levels and the way it changes the rat's behavior remain unknown.
The emerald cockroach wasp alters behavior through the injection of venom directly into the host's brain, causing hypokinesia. This is achieved by a reduction in dopamine and octopamine activity, which affects the transmission of interneurons involved in the escape response; while the host's brain circuitry responsible for movement control is still functional – and indeed it will slog along when pulled by the wasp – the nervous system is in a depressed state. Put differently: the wasp's toxin affects not the host's ability to move, but its motivation to do so.
The original function of such secretions may have been to suppress the immune system of the host, as described above. The trematode Schistosoma mansoni secretes opioid peptides into the host's bloodstream, influencing both its immune response and neural function. Other sources suggest a possible origin in molecular mimicry.
Other mechanisms
Mermithid nematodes infect arthropods, residing in their haemocoel (circulatory cavity) and manipulating their hemolymph osmolality to trigger water-seeking behavior. The means by which they do so are unknown.
Evolution
Addition of intermediate hosts
For complex life cycles to emerge in parasites, the addition of an intermediate host species must be beneficial, i.e. result in a higher fitness. It is probable that most parasites with complex life cycles evolved from simple life cycles; the evolution from simple to complex life cycles has been analyzed theoretically, and it has been shown that trophically transmitted parasites (parasites that transmit from a prey host to a predator host during predation) can be favored by the addition of an intermediate prey host if the population density of the intermediate host is higher than that of the definitive host. Additional factors that catalyze this transfer are high predation rates, and a low natural mortality rate of the intermediate host.
Parasites with a single host species are faced with the problem of not being able to survive in higher trophic levels and therefore dying with their prey host. The development of complex life cycles is most likely an adaptation of the parasite to survive in the predator. The development of parasite increased trophic transmission is a further adaptation in relation to a complex life cycle, where the parasite increases its transmission to a definitive host by manipulating its intermediate host.
Evolution of induced behaviors
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. laeviss definitive hosts. The induced behavioral change in the host thus leads to the parasite's increased success in completing its life cycle. In general, whether a specific behavioral change serves an adaptive purpose for the parasite, the host, or both, depends on the entire "host-parasite system": the life cycle of the pathogen, its virulence and the host's immune response.
Conversely, evolved behaviors of the host may be a result of adaptations to parasitism.
Taxonomic range
Parasites may alter hosts' behaviors in ways that increase their likelihood of transmission (e.g. by the host being ingested by a predator) result in the parasite's release at appropriate sites (e.g. by changes in the host's preferences for habitats) increase parasite survival or the host's likelihood of being infected with more parasites.
Viruses
Viruses from the family Baculoviridae induce in their hosts changes to both feeding behavior and environment selection. They infect moth and butterfly caterpillars, which, some time following infection, begin to eat incessantly, providing nutrients for the virus's replication. When the virions (individual virus particles) are ready to leave the host, the caterpillar climbs progressively higher until its cells are induced to secrete enzymes that liquefy the body, releasing clumps of tissue and viral material that fall to be ingested by future hosts.
Rabies is a disease caused by viruses of the Lyssavirus genus, which are released into a host's saliva and transmitted when it comes in contact with an other animal's mucous membranes or open wounds. The disease causes the host to become aggressive and prone to attacking or biting others; this, along with increased salivation, increases the chances of it spreading to new hosts. At the same time, the host experiences hydrophobia (fear of water) and laryngeal spasms.
Protozoa
The malaria parasite Plasmodium falciparum, carried by the Anopheles gambiae mosquito, changes its host's attraction to sources of nectar so as to increase its sugar intake and enhance the parasite's chance of survival. It decreases the host's attraction to human blood while gestating, only to increase it when it is ready to be transmitted to a human host.