Parasite manipulation of brain monoamines in California killifish ( Fundulus parvipinnis ) by the trematode Euhaplorchis californiensis

Abstract

California killifish (Fundulus parvipinnis) infected with the brain-encysting trematode Euhaplorchis californiensis display conspicuous swimming behaviours rendering them more susceptible to predation by avian final hosts. Heavily infected killifish grow and reproduce normally, despite having thousands of cysts inside their braincases. This suggests that E. californiensis affects only specific locomotory behaviours. We hypothesised that changes in the serotonin and dopamine metabolism, essential for controlling locomotion and arousal may underlie this behaviour modification. We employed micropunch dissection and HPLC to analyse monoamine and monoamine metabolite concentrations in the brain regions of uninfected and experimentally infected fish. The parasites exerted density-dependent changes in monoaminergic activity distinct from those exhibited by fish subjected to stress. Specifically, E. californiensis inhibited a normally occurring, stress-induced elevation of serotonergic metabolism in the raphae nuclei. This effect was particularly evident in the experimentally infected fish, whose low-density infections were concentrated on the brainstem. Furthermore, high E. californiensis density was associated with increased dopaminergic activity in the hypothalamus and decreased serotonergic activity in the hippocampus. In conclusion, the altered monoaminergic metabolism may explain behavioural differences leading to increased predation of the infected killifish by their final host predators.

Personality differences in two minnow populations that differ in their parasitism and predation risk

“…This may cause manipulative effects as a means of increased boldness and thus lead to increased predation by the definitive avian host. However, unlike the parasite-host system of brain trematode Euhaplorchis californiensis in killifish Fundulus parvipinnis (Lafferty and Morris, 1996;Shaw et al, 2009), the behavioral manipulation of D. phoxini metacercariae in minnows in the other populations has never been tested quantitatively but only described briefly (Dönges, 1969;Kekäläinen et al, 2014a). Possible predation susceptibility increasing behaviors of D. phoxini -infected host minnows nor possible mechanisms of behavioral manipulation by D. phoxini have not been examined in detail.…”

Comparing mechanisms of host manipulation across host and parasite taxa

“…Rodlet cells are thought to be a part of a larger inflammatory response that includes increased vascularization and a proliferation of fibroblasts to the site of injury (Matisz et al, 2010). The latter is intriguing when considering that brain-encysting E. californiensis metacercariae express three types of fibroblast growth factors on the surface of their cysts (Shaw et al, 2009). Fibroblast growth factors stimulate proliferation of fibroblasts, cells that are ubiquitous in all types of connective tissues and produce collagen proteins and other components of the extracellular matrix.…”

“…Parasite-induced changes in OA, DA and 5-HT feature prominently in host-parasite systems of various taxa, which indicate a significant level of evolutionary conservation in the structure and function of these chemicals (Libersat and Pflueger, 2004;Pflüger and Stevenson, 2005;Weiger, 1997;Winberg and Nilsson, 1993; see also Helluy, 2013;Libersat and Gal, 2013;McConkey et al, 2013;Vyas, 2013;Webster et al, 2013). In comparison, EP and NE have not yet been shown to be significant in altered host behaviors (Helluy and Holmes, 1990;Øverli et al, 2001;Shaw et al, 2009;Stibbs, 1985). For this reason, we focus on OA, 5-HT and DA.…”

“…This increased susceptibility to predation by birds might be due to a parasite-induced suppression of the fish's stress response. Interestingly, E. californiensis metacercariae aggregate on the brainstem in low-intensity infections (Shaw et al, 2009). Brain-encysting cercariae navigate to the brain along spinal nerves and would therefore enter the brainstem first, facilitating encystment on the brainstem (Hendrickson, 1979).…”

Parasite manipulation of host personality and behavioural syndromes

“…In many cases, however, it is possible that altering a single neurotransmitter or hormone can have cascading repercussions on several linked behavioural traits (Adamo, 2002;Shaw et al, 2009), or that inducing compensatory responses in the host can result in changes to several traits at little cost to the parasite (Lefèvre et al, 2008). In cases like these, behavioural syndromes could be prime targets for host manipulation.…”