Investigating candidate neuromodulatory systems underlying parasitic manipulation: concepts, limitations and prospects

Abstract

SummaryStudies addressing the functional basis of parasitic manipulation suggest that alteration of the neuromodulatory system is a common feature of manipulated hosts. Screening of the neuromodulatory system has so far been carried out by performing ethopharmacological analysis, biochemical quantification of neurotransmitters and neuromodulators, and/or immunocytochemistry. Here, we review the advantages and limitations of such approaches through the analysis of case studies. We further address whether the analysis of candidate neuromodulatory systems fits the current view of manipulation as being multidimensional. The benefits in combining ethopharmacology with more recent molecular tools to investigate candidate neuromodulatory pathways is also emphasized. We conclude by discussing the value of a multidisciplinary study of parasitic manipulation, combining evolutionary (parasite transmission), behavioural (syndrome of manipulation) and neuroimmunological approaches.

Parasites: evolution’s neurobiologists

“…Both intra-and extra-CNS parasites of gammarids alter the host's serotonergic neurotransmitter system (Adamo, 2012;Helluy, 2013;Perrot-Minnot and Cézilly, 2013). This effect is thought to be caused by a neuropharmacological agent secreted by the parasites (Helluy, 2013;Perrot-Minnot and Cézilly, 2013).…”

“…This effect is thought to be caused by a neuropharmacological agent secreted by the parasites (Helluy, 2013;Perrot-Minnot and Cézilly, 2013). Gammarids are crustaceans, and serotonin is a key neuromodulator mediating their escape behaviours (Weiger, 1997).…”

“…Escape behaviours are altered in infected gammarids, making them more prone to predation by the definitive host (Helluy, 2013). Pharmacological manipulations of the serotonergic system of infected and uninfected gammarids suggest that the changes in serotonin are causally related to the change in behaviour (Helluy, 2013;Perrot-Minnot and Cézilly, 2013). However, nonserotonergic mechanisms appear to be involved as well, at least for trematode infections (Helluy and Thomas, 2010;Helluy, 2013).…”

“…Parasites typically use less energetically expensive methods to alter host neurochemistry. For example, in infected gammarids, a variety of phylogenetically diverse parasites are thought to induce the host to increase serotonin production within its CNS, reducing the direct cost to the parasite (Lefèvre et al, 2009;Adamo, 2012;Helluy, 2013;Perrot-Minnot and Cézilly, 2013). The parasitic wasp C. congregata reduces the breakdown of the neuromodulator octopamine, increasing the time levels are elevated in the host, without the parasite having to continuously secrete large amounts of this biogenic amine (Adamo, 2005).…”

Animal personality and state–behaviour feedbacks: a review and guide for empiricists

“…For example, behaviour-parasite feedbacks (discussed below) are often mediated by effects of parasites on host hormone levels [41,42] and, in some cases, appear to involve adaptive parasite manipulation of host neuroendocrine pathways [43,44]. Progress in understanding feedbacks between behaviour and multiple, interacting components of the overall neuroendocrine system should be invaluable for better understanding personalities.…”