Behavioral Interactions between Parasites and Hosts: Host Suicide and the Evolution of Complex Life Cycles

Parasites and their hosts show behavioral as well as physiological interactions. Parasites are able to alter the behavior of their hosts, and hosts in turn may employ behavioral retaliation in response to parasitic infection. The four types of endoparasites discussed in the paper are parasitoids (group 1), parasitic castrators (group 2), single-host true parasites (group 3) and multihost true parasites (group 4). For each of these four types of parasites the role of parasite induced modifications of host behavior is analyzed with respect to (1) dispersal of the parasite propagules to new hosts, (2) modification of the host's energy budget to provide energy for the parasite's growth and maturation, and (3) keeping the host alive until the parasite has completed its life cycle. It is found that modification of the host's energy budget is profitable for parasitoids and castrators, but not for group 3 parasites. During some stages of its life cycle the group 4 parasite can employ modification of the host's energy budget, but only if the larval parasite resembles parasitoids or castrators in certain ways. Modification of host behavior to facilitate dispersal of propagules to new hosts, or to the next host in a series of hosts, should be employed most often by the intermediate larval stages of group 4 parasites. The reproductive fitness of the host is reduced by its parasitic load. A parasitoid or castrator may reduce the host's reproductive fitness to zero, while a single- or multiple-host true parasitic infection may scarcely impair it. A host may defend itself by preventing infection, or, once infected it can protect its kin by attempting to prevent their infection. Host suicide is the term coined to describe aberrant behavior on the part of an infected host which leads to increased probability of death by predation. Host suicide will increase the inclusive fitness of the host if (1) the suicide prevents the maturation of the parasite; (2) the mature parasite is more likely to infect the host's kin than nonkin; and (3) the benefit to the host, in terms of the increased fitness of the kin, is greater than the cost of the suicide, measured in terms of the loss of the host's own reproductive fitness. Host suicide is most profitable when the host is infected by a parasitoid. The parasitoid reduces the host's reproductive fitness to zero, so that the cost of the suicide is also zero. Suicide is of variable value when the host is infected by a castrator, the value depending on the degree to which the parasitoid reduces the host's reproductive fitness. Host suicide is not expected when the host is infected with group 3 or 4 parasites. Mature parasitoids may be more likely to infect the host's kin than nonkin in social or colonial animals, or in species with small, isolated, inbred populations. The similarity between host suicide and the passage of group 4 parasites from intermediate hosts to definitive hosts is noted, and the possible role of host suicide in the evolution of such complex parasitic life cycles is examined.