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Animals have a number of behavioral defenses against infection. For example, they typically avoid sick conspecifics, especially during mating. Most animals also alter their behavior after infection and thereby promote recovery (i.e., sickness behavior). For example, sick animals typically reduce the performance of energetically demanding behaviors, such as sexual behavior. Finally, some animals can increase their reproductive output when they face a life-threatening immune challenge (i.e., terminal reproductive investment). All of these behavioral responses probably rely on immune/neural communication signals for their initiation. Unfortunately, this communication channel is prone to manipulation by parasites. In the case of sexually transmitted infections (STIs), these parasites/pathogens must subvert some of these behavioral defenses for successful transmission. There is evidence that STIs suppress systemic signals of immune activation (e.g., pro-inflammatory cytokines). This manipulation is probably important for the suppression of sickness behavior and other behavioral defenses, as well as for the prevention of attack by the host's immune system. For example, the cricket, Gryllus texensis, is infected with an STI, the iridovirus IIV-6/CrIV. The virus attacks the immune system, which suffers a dramatic decline in its ability to make proteins important for immune function. This attack also hampers the ability of the immune system to activate sickness behavior. Infected crickets cannot express sickness behavior, even when challenged with heat-killed bacteria. Understanding how STIs suppress sickness behavior in humans and other animals will significantly advance the field of psychoneuroimmunology and could also provide practical benefits., (© The Author 2014. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology. All rights reserved. For permissions please email: journals.permissions@oup.com.)

For millions of years, parasites have altered the behaviour of their hosts. Parasites can affect host behaviour by: (1) interfering with the host's normal immune-neural communication, (2) secreting substances that directly alter neuronal activity via non-genomic mechanisms and (3) inducing genomic- and/or proteomic-based changes in the brain of the host. Changes in host behaviour are often restricted to particular behaviours, with many other behaviours remaining unaffected. Neuroscientists can produce this degree of selectivity by targeting specific brain areas. Parasites, however, do not selectively attack discrete brain areas. Parasites typically induce a variety of effects in several parts of the brain. Parasitic manipulation of host behaviour evolved within the context of the manipulation of other host physiological systems (especially the immune system) that was required for a parasite's survival. This starting point, coupled with the fortuitous nature of evolutionary innovation and evolutionary pressures to minimize the costs of parasitic manipulation, likely contributed to the complex and indirect nature of the mechanisms involved in host behavioural control. Because parasites and neuroscientists use different tactics to control behaviour, studying the methods used by parasites can provide novel insights into how nervous systems generate and regulate behaviour. Studying how parasites influence host behaviour will also help us integrate genomic, proteomic and neurophysiological perspectives on behaviour.

Neuromodulators can resculpt neural circuits, giving an animal the behavioral flexibility it needs to survive in a complex changing world. This ability, however, provides parasites with a potential mechanism for manipulating host behavior. This paper reviews three invertebrate host-parasite systems to examine whether parasites can change host behavior by secreting neuromodulators. The parasitic wasp, Cotesia congregata, suppresses host feeding partly by inducing the host (Manduca sexta) to increase the octopamine concentration in its hemolymph. The increased octopamine concentration disrupts the motor pattern produced by the frontal ganglion, preventing the ingestion of food. Polymorphus paradoxus (Acanthocephalan) alters the escape behavior of its host, Gammarus lacustris (Crustacea), possibly through an effect on the host's serotonergic system. The trematode Trichobilharzia ocellata inhibits egg-laying in its snail host (Lymnaea stagnalis), partly by inducing the host to secrete schistosomin. Schistosomin decreases electrical excitability of the caudodorsal cells. The parasite also alters gene expression for some neuromodulators within the host's central nervous system. In at least two of these three examples, it appears that the host, not the parasite, produces the neuromodulators that alter host behavior. Producing physiologically potent concentrations of neuromodulators may be energetically expensive for many parasites. Parasites may exploit indirect less energetically expensive methods of altering host behavior. For example, parasites may induce the host's immune system to produce the appropriate neuromodulators. In many parasites, the ability to manipulate host behavior may have evolved from adaptations designed to circumvent the host's immune system. Immune-neural-behavioral connections may be pre-adapted for parasitic manipulation., (Copyright 2003 S. Karger AG, Basel)