quantitative predictions. Given that the bulk of the published empirical
work on host manipulation by parasites consists of investigations into
whether a particular parasite shows signs of being a manipulator or not,
optimality theory could at least serve to focus efforts on quantitative
hypothesis testing, rather than simply adding to existing lists of
manipulating species.
The second cornerstone of modern behavioural ecology is the concept
of evolutionarily stable strategies (ESS), derived from game theory
(Maynard Smith, 1982). It states that the optimal strategy for an individual
in any given situation depends on the strategies adopted by other individ-
uals in the population. The ESS are the mixture of strategies in the
population where the net reproductive pay-off to all strategies is the same.
The ESS can be a stable ratio of different genotypes, or they can consist of
each individual adopting the different strategies for stable proportions
of their time. The outcome is that no other feasible alternative strategy can
invade an evolutionarily stable population.
This concept has applications in the area of host manipulation.
In certain host-parasite systems, there is usually only one parasite per
host, and that parasite must manipulate the behaviour of its host on
its own. When more than one individual parasite ends up in the same
intermediate host, they may all incur additional costs because of limited
space or other resources in the host (e.g. Dezfuliet al., 2001). In other
systems, however, several conspecific parasites normally share the
same intermediate host. In these cases, the optimal group investment in
manipulation can be modelled using an optimality approach (Brown,
1999). We might expect the cost of manipulation to be shared by
all co-occurring parasites, such that the investment of any individual
is inversely proportional to the size of the group it belongs to. Large
numbers of parasites in the same intermediate host also introduce the
possibility of cheating. In a large group, a parasite that invests less in
manipulation than its expected share can reap all the benefits of manipu-
lation without paying the full costs (Poulin, 1994). As seen above for the
trematodesD. dendriticumandM. papillorobustus, one parasite can pay
the full costs and receive no benefits, while the others get all the benefits
at no cost. Not all parasites in a population adopt the same strategy. An
ESS approach is ideal for studying the ratio of the two strategies, honest
(manipulative) and cheating (non-manipulative), in the parasite popula-
tion. When cheaters are more common than their ESS proportion, their
relative fitness would decrease because there are not enough manipula-
tors present to guarantee an increase in the transmission rate, and their
frequency will return to the ESS. If the proportion of manipulators
increases above the ESS, the few cheaters left achieve greater fitness by
paying even lower costs and their success leads to their proportion return-
ing to the ESS. Thus we may expect a stable equilibrium ratio of honest
and cheating parasites. Accurate quantitative predictions are difficult to
make but should be possible when knowledge of the costs in particular
systems is available.Parasite Manipulation of Host Behaviour 249