Mechanisms of Manipulation
Surely one of the most convincing pieces of evidence that a parasite is
truly manipulating the behaviour of its host, and not merely causing a
non-adaptive pathological behaviour, would be finding a parasite organ
whose sole purpose is the induction of the behavioural change in the host
(Poulin, 1995). The existence of such an organ could only be accounted
for by natural selection favouring individuals possessing the organ over
ones that do not. There is a growing body of information on the nature
of the mechanisms used by parasites to alter the behaviour of their
hosts (reviewed by Holmes and Zohar, 1990; Hurd, 1990; Beckage, 1991;
Thompson and Kavaliers, 1994; Kavalierset al., 2000). Knowledge of the
mechanisms involved, however, is still limited to a few host–parasite
systems, and it lags behind knowledge of the actual effects on host
behaviour.
In some systems, chemical modulation of host behaviour is the
method employed by the parasite (Hurd, 1990; Beckage, 1991). This
is particularly well documented in interactions between parasitoids
and their insect hosts (Beckage, 1985, 1993; Eberhard, 2000), but is also
known from systems involving helminths. For instance, in the case of the
previously mentioned acanthocephalanP. paradoxusand the photophilic
behaviour it induces in its amphipod host, Helluy and Holmes (1990)
have shown that an identical response can be elicited by chemicals with-
out the need for infection. Thus the way in which the parasite achieves
manipulation is by altering host chemistry through its own secretions.
The trematodeM. papillorobustus, which causes a similar photophilia in
its amphipod host, apparently also achieves this via chemicals, though
the evidence is more circumstantial (Thomaset al., 2000).
The production of modulating chemicals or any other active alteration
of host physiology is not always necessary for a parasite to modify host
behaviour. Certain parasites have adopted a potentially cheaper method,
consisting simply of encysting in a particular tissue of the intermediate
host. For instance, the presence of larval parasites in either the nervous
system (Crowden and Broom, 1980; Lafferty and Morris, 1996; Barber and
Crompton, 1997), lungs (Rau and Caron, 1979) or muscles (Rau and
Putter, 1984; Thomas and Poulin, 1998) of certain intermediate hosts
is sufficient to change their behaviour in ways that render them more
susceptible to capture by the definitive host. In these systems, natural
selection has increased the site selectivity of the parasite to ensure it
benefits from higher transmission success at virtually no cost beyond
those associated with reaching the infection site.
A complex phenomenon such as host manipulation by parasites
must be investigated at both the proximate and ultimate levels. In other
words, the phenomenon can only be truly understood if we know the
mechanisms that lead to a change in host behaviour as well as the fitness
consequences for the parasite. For some reason, we know which host
behaviours are changed in a large number of host–parasite associations,Parasite Manipulation of Host Behaviour 253