Abstract
Parasite fitness is often tied closely to host behaviour, especially when transition to a definitive host or egression in a particular environment is involved. Thus natural selection has driven many parasites to control host behaviour to varying extent. How parasites alter and/or create behaviour is a fascinating question from neuroethological and physiological perspectives, and much could be gained from a complete answer.
A review of the literature (chapter 2) reveals this untapped potential is offset by the difficulty involved in disentangling the host's response to infection from the parasite's active manipulation of behaviour. Establishing causation between the parasite and observed changes in host physiology, via the identification of manipulative factors, is the next step forward. Yet, moving from correlation to causation is a difficult step to take. Convergent and ontogenetic evidence is very rare in the literature, and while still correlational, it can provide strong evidence for adaptive host manipulation.
Hairworms (phylum Nematomorpha) and mermithids (phylum Nematoda) infecting arthropods induce hydrophilia in their hosts, forcing them to water, which is essential for the worms' survival after egression. The mechanisms behind this behavioural change have been investigated in hairworms, but not in mermithids. Using a water choice behavioural test (chapter 3) followed by a proteomic investigation (chapter 4) into the brains of Forficula auricularia (earwig) and Bellorchestia quoyana (sandhopper), infected with the mermithids Mermis nigrescens and Thaumamermis zealandica respectively, evidence for adaptive manipulation was contrasted against proteomic results from hairworm-infected hosts.
In the behavioural test, earwigs infected by mature worms drowned themselves in water significantly more frequently than uninfected individuals or those harbouring small worms; no such pattern was found for sandhoppers. Across both hosts (and hairworm-infected hosts, from earlier studies), the general function of regulated proteins was conserved. Proteins involved in energy generation/mobilization were up/down regulated across sandhoppers and earwigs, corroborating reports of erratic/hyperactive behaviour in infected hosts, which may be involved in getting to water. Mtpalpha, a key component in energy mobilization, was regulated across all hosts suggesting it may be a crucial factor in inducing hyperactivity.
Regulated proteins involved in axon/dendrite and synapse modulation were also common to all hosts, suggesting neuronal manipulation is involved in hydrophilia. Clathrin, a fundamental component of neurotransmitter release, was regulated across all infected hosts (like Mtpalpha), also suggesting neuronal manipulation. Furthermore, down-regulation of CamKII and associated proteins suggest manipulation of memory also participates in the behavioural shift. Only a subset of all neuron-related proteins were found in sandhoppers infected with long worms; combined with results of the behavioural tests, this suggests Thaumamermis zealandica may have lost this component of the hydrophilic manipulation.