Behavior-altering parasite
Behavior-altering parasites are
Among the behavioral changes caused by parasites is carelessness, making their hosts easier prey.[6][4] The protozoan Toxoplasma gondii, for example, infects small rodents and causes them to become careless and may even cause them to become attracted to the smell of feline 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).[7]
Examples
Parasite manipulations can be either direct or indirect. Indirect manipulation is the most frequent method used by behavior-altering parasites,[8] 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.[9] Affecting the host's neural system is complicated and manipulation includes initiating immune cascades in the host.[10] 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.[9] A direct approach to behavioral manipulation is often very costly for the parasite,[9] 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[8] to create the necessary neuroactive compounds to induce a desired behavioral response.[9] Parasites can also indirectly affect the behavior of their hosts by disturbing their metabolism, development, or immunity.[9] Parasitic castrators drastically modify their hosts' metabolism and reproduction, sometimes by secreting castrating hormones, changing their behavior and physiology to benefit the parasite.[11]
Viruses
Baculoviridae
Viruses from the family Baculoviridae induce in their hosts changes to both feeding behavior and environment selection. They infect moth and butterfly caterpillars, who some time following infection begin to eat incessantly, providing nutrients for the virus's replication. When the virions (virus "units") are ready to leave the host, the caterpillar climbs higher and higher, until its cells are made to secrete enzymes that "dissolve the animal into goo", raining down clumps of tissue and viral material for ingestion by future hosts.[13]
Lyssavirus
Protozoal parasites
Plasmodium falciparum
The malaria parasite 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.[16] It also decreases the host's attraction to human blood while gestating,[13] only to increase it when it is ready to be transmitted to a human host.[13][17]
Toxoplasma gondii
The protozoan
Parasitic helminths
Multiple parasites increase their host's risk of predation to facilitate their transition from their intermediate host to their definitive host, including: Euhaplorchis californiensis,[20] Dicrocoelium dendriticum,[20] Diplostomum pseudospathaceum,[citation needed] and Myrmeconema neotropicum.[21]
Dicrocoelium dendriticum
The lancet liver fluke (Dicrocoelium dendriticum) is a parasitic trematode with a complex life cycle. In its adult state it occurs in the liver of its definitive host (ruminants), where it reproduces. The parasite eggs are passed with the feces of the host, which then are eaten by a terrestrial snail (first intermediate host). The fluke matures into a juvenile stage in the snail, which in an attempt to protect itself excretes the parasites in "slime-balls". The "slime-balls" are then consumed by ants (second intermediate hosts). The fluke manipulates the ant to move up to the top of grass, where they have a higher chance of being eaten by grazing ruminants.[20]
Leucochloridium paradoxum
The trematode Leucochloridium paradoxum matures inside snails of the genus Succinea. When ready to switch to its definitive host, a bird, the parasite travels to the eye stalks of its host and begins to pulsate, attracting birds with its striking resemblance to an insect larva.[22] It also influences the normally nocturnal snail to climb out into the open during the day for an increased chance of being consumed by a bird.[23]
Microphallus
The parasitic
Myrmeconema neotropicum
The parasitic nematode Myrmeconema neotropicum infects the intermediate ant host Cephalotes atratus. The nematode then induces a morphological change in the ant, which turns the gaster color from black to red, making it resemble fruit. This color transition makes the ant susceptible to predation by frugivorous birds, which act as the parasite's definitive hosts. The parasitic eggs are deposited in the bird's feces and are eaten by ants, which complete the cycle.[21]
Nematomorpha
Crickets infected by horsehair worms (Nematomorpha) exhibit light-seeking behavior and increased walking speed, leading them to open spaces and ponds (the surface of which reflects moonlight); the crickets will eventually find and enter a body of water, where the worm will wiggle out of the cricket's abdomen and swim away. While crickets often drown in the process, those who survive exhibit a partial recovery and return to normal activities in as little as 20 hours.[25]
Schistocephalus solidus
Schistocephalus solidus is a parasitic flatworm with three different hosts, two intermediate and one definitive. In its adult stage the tapeworm resides in the intestine of piscivorous birds, where they reproduce and release eggs through the bird's feces. Free-swimming larvae hatch from the eggs, which are in turn ingested by copepods (the first intermediate host). The parasite grows and develops in the crustacean into a stage that can infect the second intermediate host, the three-spined stickleback (Gasterosteus aculeatus).[26] The parasite's definitive host, a bird, then consumes the infected three-spined stickleback and the cycle is complete. It has been observed that S. solidus alters the behavior of the fish in a manner that impedes its escape response when faced with a predatorial bird.[27] This parasite-induced behavioral manipulation effectively increases the chance of it being consumed by its definitive bird host. It has also been observed that the parasite does not induce this behavior until it has reached a developed stage that can survive in the host bird[27] and therefore effectively reduce its own mortality rate, due to premature transmission.[citation needed]
Parasitic and Parasitoid insects
Ampulex compressa
The
Dinocampus coccinellae
The wasp
Hymenoepimecis argyraphaga
The parasitic wasp Hymenoepimecis argyraphaga grows its larvae on spiders of the species Leucauge argyra. Shortly before killing its host the larva injects it with a chemical that changes its weaving behavior,[34] causing it to weave a strong, cocoon-like structure. The larva then kills the spider and enters the cocoon to pupate.[35]
Ophiocordyceps unilateralis
A similar, but much more intricate behavior is exhibited by ants infected with the fungus
Phoridae
Several species of fly in the family
Reclinervellus nielseni
The parasitic wasp larvae Reclinervellus nielseni attach to the spider Cyclosa argenteoalba, releasing substances that modify the spider's web-building behavior so that it weaves a cocoon-like structure for the larvae to pupate in. This manipulated behavior was longer lasting and more prominent the longer the larvae were attached to the spider.[43]
Strepsiptera
Strepsiptera of the family Myrmecolacidae 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).[44]
Parasitic crustaceans
Rhizocephala
Members of the order Rhizocephala such as Sacculina carcini alter male hosts' hormonal balance, to encourage nurturing behavior similar to that seen in females. The parasite usually spends its entire life within the host; however, if it is removed from the host in a laboratory setting, male hosts will subsequently grow partial or complete female gonads.[45]
Mechanisms
The way in which parasites induce behavioral changes in hosts has been compared to the way a neurobiologist would effect a similar change in a lab.[46] 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.[47]
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.[47]
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.[48] 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.[46]
Altered neurotransmission
Parasites that induce behavioral changes in their hosts often exploit the regulation of social behavior in the brain.
The emerald cockroach wasp alters behavior through the injection of venom directly into the host's brain, causing hypokinesia.[28][47] This is achieved by a reduction in dopamine and octopamine activity, which affects the transmission of interneurons involved in the escape response;[29] so 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
Other mechanisms
Evolutionary perspective
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.[53][54] It is probable that most parasites with complex life cycles evolved from simple life cycles;[55] 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.[55] Additional factors that catalyze this transfer are high predation rates, and a low natural mortality rate of the intermediate host.[55]
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.[4] 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.[53]
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
Conversely, evolved behaviors of the host may be a result of adaptations to parasitism.[57]
See also
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