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Some parasites and parasitoids cause changes in the behavior of their hosts. There are two types of parasite-induced behavioral changes: parasitic manipulation of host behavior and host defense against parasites. The evolutionary origins of these behavioral changes have been the topic of theoretical discussion. Many parasite-induced behavioral changes may be the product of coevolution between hosts and parasites, but the extent to which specific alterations can be considered adaptive is frequently debated.

Adaptation and the Host-Parasite Relationship
The evolutionary arms race between parasites and hosts involves a series adaptations and counter-adaptations. Parasite-induced behavioral changes in a host are considered adaptive when the behaviors have evolved to increase the fitness of either the host or the parasite. For example, ants (Cephalotes atratus) infected with a parasitic nematode are transformed to resemble a ripe fruit. This physical change is accompanied by behavioral changes that increase the ants’ conspicuousness to prey. Together, these alterations increase the ants’ risk of predation by birds. Because ants are the intermediate hosts of the parasite while birds are the definitive hosts, this predation allows the parasite to complete its life cycle. The nematode’s manipulation of ant appearance and behavior thus confers fitness benefits onto the parasite. Hosts may also alter their own behavior in the presence of parasites to defend themselves or to compensate for the deleterious impacts of infection. For example, freshwater snails (Biomphalaria glabrata) exposed to the parasitic trematode Schistosoma mansoni tend to produce more eggs than snails that are not exposed. Because the fecundity of the snail decreases with time post-infection, this initial increase in egg production allows the snail to compensate for possible impending costs of infection.

Frequently, any changes observed in infected hosts are assumed to be adaptive for either the parasite or the host. As a result, the term adaptation is often used loosely to describe any changes that occur in a host following infection. To introduce rigor to this term, theorists have outlined four criteria that characterize adaptation in the context of parasite-induced behavioral changes.

Parasite-induced behavioral changes should satisfy four conditions to be considered adaptive.


 * Fitness effects- Fitness benefit is the most important criterion for adaptation. The induced behavioral change must increase fitness of either the host or the parasite in order to be considered adaptive.
 * Correlation between the trait and its fitness benefits- A strong correlation between the induced behavioral change and the benefit to the host or parasite is evidence for adaptation.
 * Convergence - Similar traits arising in different lineages experiencing similar selective pressures is considered evidence of adaptation.
 * The complexity of the trait- A trait that appears too intricate to have appeared merely by chance or as a by-product of another selective force may be an adaptation. The evolution of such a trait is assumed to have required the organizing principle of selection.



It is important to note that these criteria are not foolproof; instead, they are guidelines to help characterize parasite-induced behavioral changes as either adaptive or coincidental. Behavioral complexity is subjective, and a judgment of the intricacy of a behavior may not take into account the complexity of the underlying mechanisms. A trait whose expression appears simple may be mechanistically complex. Additionally, fitness benefits are difficult to quantify: benefits may be statistically negligible but significant enough for natural selection to act upon. While these limitations are of practical concern, they should not deter research that attempts to assess the evolution of parasite-induced behavioral changes. Research that creatively addresses the criteria for adaptation is needed to improve our understanding of how behavioral traits have evolved under the selective pressures inherent to the parasite-host relationship.

Parasitic Manipulation of Host Behavior
Many parasites induce behaviors in their hosts that appear to confer fitness benefits unto themselves. Commonly cited examples include behaviors that enhance the likelihood of parasite transmission from host to host, changes in host preferences for habitat selection that result in parasite release at appropriate sites, and behavioral changes that increase the host’s likelihood of colonization by suitable mates for the parasite. Such behavioral changes are generally categorized using one of two mutually exclusive hypotheses: the adaptive manipulation hypothesis or the coincidental byproduct hypothesis.

Adaptive Manipulation
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. Here, extended phenotype refers to the fact that the genes of the parasite influence the phenotype of the host. Few studies have managed to provide sufficient evidence for adaptation using the criteria discussed above, but establishing a direct link between parasitic manipulation and increased life history success of a parasite is critical to doing so, given that fitness benefits are considered the most important criterion for adaptation. Many behaviors induced by obligate parasites to complete their lifecycles are considered to be examples of adaptive manipulation because of their clear relationship to parasite fitness. For example, evidence has demonstrated that infection by the parasite Pomphorhynchus laevis leads to altered drifting behavior in Gammarus pulex, an intermediate host of P. laevis. This altered behavior increases G. pulex’s predation risk by P. laevis’s definitive host. The induced behavioral alteration in the host thus leads to the parasite’s increased success in completing its life cycle. The establishment of a direct link between the parasite-induced behavioral alteration and the success of the parasite is convincing evidence of the adaptive manipulation hypothesis.

Coincidental Byproduct Hypothesis
The coincidental byproduct hypothesis accounts for parasite-induced behavioral alterations that are merely pathological side effects of infection or ancestral legacies that no longer meet the criteria for adaptation in a modern context. Given the complexity of providing evidence of adaptation, the coincidental byproduct hypothesis is often the simplest explanation for behavior changes in hosts following parasite infection. Although the principle of parsimony has been used to defend the coincidental byproduct hypothesis, the legitimacy of this defense has been questioned due to the difficulty of proving the absence of benefit. Behavioral alterations that would be considered coincidental byproducts include pathological side effects of infection with no benefits for the parasite, pathological side effects with coincidental fitness benefits for the parasite and side effects of other manipulative adaptations that have coincidental benefits for the parasite. For example, when honeybees (Apis mellifera) are infected with the parasite Nosema ceranae, they demonstrate behavioral fever, or a change in thermal preference. Although this response appears to be an adaptive manipulation on the part of the parasite, which reproduces more successfully at higher temperatures, there is evidence that the response is a coincidental by-product. The proximate mechanism of the behavioral fever appears to be a pathological response to infection: the bees have poor thermoregulatory ability due to decreased energy during infection and thus seek out warmer microclimates, which coincidentally benefits the parasite.

Due to the difficulties of categorizing parasite-induced behaviors as adaptive or as coincidental byproducts, further research that rigorously attempts to evaluate behaviors based upon criteria for adaptation is needed. This is of particular importance for understanding the extent to which the coevolution of hosts and parasites has led to the current diversity of behavior in the animal kingdom.

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. A scientist may stimulate a certain pathway, either mechanically or chemically, in order to produce a specific behavior, such as increased appetite or lowered anxiety. Parasites also produce specific behavioral changes in their hosts. Rather than stimulating specific neurological pathways, however, parasites appear to target broader areas of the central nervous system (CNS). While the proximate mechanisms underlying this broad targeting have not been fully characterized, two mechanisms used by parasites to alter social behavior in their vertebrate hosts have been identified: infection of the CNS and altered neurochemical communication.

Infection of the Central Nervous System
Some parasites alter host behavior by infecting neurons in the host’s CNS. The host’s CNS 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 CNS inflammation in their hosts include Toxoplasma gondii in rats, Trypanosoma cruzi in mice, and Plasmodium mexicanum in the Mexican lizard.

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

Altered Neurochemical Communication
Parasites that induce social-behavioral changes in their hosts often exploit the regulation of social behavior in the brain. Social behavior is regulated by hormones, such as dopamine and serotonin, in the emotional centers of the brain - primarily the amygdala and the hypothalamus. 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, infection with Toxoplasma gondii causes rats to lose their aversion to cat odor. This increases the risk of predation by cats, T. gondii’s definitive host. In order to induce the loss of aversion to cat odor in rats, a neurobiologist would target a specific neuroanatomical location in the rat, but evidence suggests that T. gondii attaches to the hypothalamus generally rather than targeting 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. The mechanistic details underlying the increase in dopamine levels and its pertinence to the induced behavioral change remain elusive.

One theory for how parasites may alter neurochemical communication in their hosts suggests that the parasites may secrete intermediate compounds that cause increases in substances involved in neurochemical communication. In mammals infected with T. gondii, for example, behavioral changes that reduce the ability to escape predation from subsequent T. gondii hosts may be induced by increases in dopamine. 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.

The mechanisms of parasite-induced altered social behavior provide evidence of adaptation in many cases. An understanding of the mechanisms allows for evaluation of the complexity of the trait and the correlation between the mechanism and the potential fitness benefits for the parasite.

Behavioral Adaptations for Parasite Resistance
Parasites often have deleterious effects on host fitness and therefore act as a potential selective force on organisms. Natural selection should favor hosts that effectively protect themselves against parasites. Using the criteria for adaptation, certain behavioral changes used by hosts may be characterized as adaptations. These behaviors include those used to eliminate and avoid parasites, such as behavioral fever and self-medication, and those that compensate for the deleterious impacts of infection.

Behavioral Fever
A well-known example of a host strategy used by ectotherms to combat infection is behavioral fever. Behavioral fever is the use of behavior to alter internal body temperature until it is outside the range observed in healthy individuals. This is usually achieved through altered microhabitat selection. Behavioral fever is an effective method of combating parasites if components of the host’s immune system function more efficiently at a certain temperatures or if the parasite’s pathogenicity decreases at temperatures outside the host’s normal physiological range.

The benefits of behavioral fever have been observed in grasshoppers (Melanoplus sanguinipes) infected with Nosema acridophagus. When infected with this protozoan parasite, grasshoppers show a preference for higher temperatures as compared to healthy grasshoppers. This behavioral fever increases the probability of survival of infected hosts. Typically, uninfected grasshoppers placed at febrile temperatures (temperatures that induce fever) experience negative growth. In infected grasshoppers, however, fever effectively combats infection, and this benefit has been shown to outweigh the costs of fever.

The fitness benefits of some instances of behavioral fever for infected hosts have justified the classification of these cases as adaptive responses.

Self-medication
The consumption of natural substances that help an organism combat parasitic infection has been observed in a number of vertebrate and invertebrate species. When animals are infected, they may alter their foraging behavior to seek medicinal plants or animals. Therapeutic benefits may be achieved through external application of medicinal substances. For example, anting behavior in birds refers to the act of rubbing crushed ants, plants, millipedes or other substances onto feathers and skin to exploit the anti-parasitic properties of these substances. In other cases, ingestion of the medicinal substance confers fitness benefits. A study conducted on chimpanzees (Pan troglodytes) in Nigeria demonstrated that individuals sometimes consume leaves and defecate them intact. The defecation of intact leaves suggests that the leaves were not ingested for nutritional purposes. Because the consumption of whole leaves occurs more frequently in the rainy season when parasite infections are more common, potential therapeutic benefits have been posited as an explanation for such behavior. Similarly, in sub-Saharan Africa, chimpanzees and humans are known to consume Vernonia amygdalina’s pith to control intestinal nematode infections.

Self-medication is a complex behavior found in multiple animal taxa, thereby meeting the complexity and convergence criteria for adaptation. Self-medication also demonstrates correlation between the trait and fitness benefits, as infected animals specifically select anti-parasitic substances that appear to increase their survival. Thus, in many cases, self-medication may be considered an adaptive host behavior.

Compensation
In the event that animals cannot eliminate a parasite, hosts may alter their behavior following infection to compensate for negative effects on their fitness. Compensation is frequently associated with reproductive behavior. For example, compensatory behavior has been observed in bush crickets (Requena verticalis) infected with gut protozoa. In the absence of infection, female bush crickets are the discriminatory sex; they choose males based on their ability to provide spermatophylax, a nutritious meal that increases female fecundity. Despite reproductive constraint, females infected with parasites attempt to mate more frequently and are less discriminating toward males than healthy females. The proposed explanation suggests that the heightened nutritional requirements of infected females can be met by the spermatophylax provided by males. Females mate more often to gain access to this additional food source.

Generally, compensatory behaviors are complex behavioral changes that can confer fitness benefits onto infected hosts. Some cases of compensation can therefore be considered adaptive.

Suicidal Behavior
When threatened with parasitic attack, hosts can increase their reproductive success by protecting themselves; however, they can also do so indirectly by protecting their kin. Kin protection has been proposed as a case of adaptive suicidal behavior in infected hosts. Kin selection theory states that an infected host can increase its inclusive fitness by lowering the risk of parasitic infection for its kin. By killing itself, the host kills the parasite, thereby reducing the chances that the parasite will infect its kin. For suicide to be considered adaptive, the increased inclusive fitness associated with suicide must exceed the loss of personal reproductive success for the host. Although the parasitized individual’s future reproductive success is reduced to zero after suicide, if kin are spared from infection as a result, the host’s genes are still passed on to the next generation. Thus, the tendency to commit suicide in the face of parasitic infection will be preserved and may spread in the population.

Suicidal behavior has been documented in pea aphids (Acyrthosiphon pisum) infected with a braconid wasp Aphidius ervi. When given the opportunity, infected pea aphids are more likely to participate in risky behavior that leads to death by a predator than non-infected aphids. This behavior has been shown to decrease the risk of offspring infection.

Host suicide thus meets the criteria for adaptation of complexity and correlation between a trait and its potential fitness benefits, though the fitness advantage from inclusive fitness has yet to be experimentally demonstrated.