Parasite-induced modifications of host behaviour are known from a wide range of host-parasite associations. In many cases, these behavioural changes are thought to be adaptive and. benefit the parasite by increasing its probability of successful transmission. However, in many cases, energy spent on host manipulation will not be available for other functions, such as growth. These trade-offs suggest that in the absence of other constraints, natural selection will optimize, and not maximize, the influence of parasites on host behaviour. This argument is developed and expanded into theoretical considerations of the evolution of host behaviour manipulation by parasites. Among populations of the same parasite species or among closely-related species, the optimal investment into manipulation, or optimal manipulative effort (ME*), of individual parasites is predicted to increase as (1) typical infrapopulation size decreases, (2) prevalence increases, (3) the longevity of the infected host, or of the parasite in its host, decreases, (4) passive transmission rates decrease, and (5) parasite fecundity decreases. This evolutionary analysis indicates that ecological and life history variables may have played an important role in the evolution of manipulation of host behaviour by parasites.

The parasitic nematode Anguillicola crassus was recently introduced into populations of the European eel, Anguilla anguilla. We investigated, under experimental conditions, the regulation of A. crassus infrapopulations. We tested the effects of (1) the resource-limited habitat of the parasite and (2) the coexistence of several developmental stages in its niche (the swim-bladder) on the composition of the infrapopulations. The results revealed that the respective effects of these factors differed substantially during the course of the infection. Third-stage larvae (L3s) establishment would not be constrained by the size of the swim-bladder. Their moult to fourth-stage larvae (L4s) would be accelerated as the number of L3s increased. The moulting time of L4s to adults would be reduced by males and would be constrained by the size of the swim-bladder. However, the moult of L4s to adults and their further development would be synchronized with those of the opposite sex. At the time of mating, the number of males and the body weight of adults would depend on the size of the swim-bladder. Soon after the laying of eggs, the developmental constraint on the late L3s would decrease. When adults die, constraints would cease and late larval stages would moult to become adults.

European eels Anguilla anguilla from the rivers Thames and Test, in the south of England, were examined between 2000 and 2003 for infection with the swim-bladder nematode Anguillicola crassus. Since its introduction to Thames eels at tidal estuarine locations circa 1987, A. crassus has become established in non-tidal freshwater stretches upriver and data from these locations are reported for the first time. The prevalence of infection at Thames estuary locations was higher during 2000–2003 than for the period 1987–1992. By 2003, similar prevalences were observed at freshwater and estuarine locations, but infection intensities were significantly higher in freshwater. Eels from the river Test appear to have been recently colonized by A. crassus (circa 2000). Parasite population establishment within these eels was uncharacteristically slow during 2000–2001, with low prevalence and intensity of infection, and few gravid females during this period. By 2003, infection levels in Test eels were similar to those in Thames eels. The expansion of the A. crassus population in Test eels has occurred in the absence of the paratenic host ruffe Gymnocephalus cernuus, and at suboptimal pH for the survival and infectivity of free-living larvae. The epidemiology of A. crassus in Test eels demonstrates that transmission of A. crassus by ruffe is not required for high prevalence and intensity of infection in eels. However, the consistently low and atypical levels of infection in Test eels during 2000 and 2001 suggests that paratenic transmission by ruffe may provide a substantial contribution to the dynamics of A. crassus in eels in the early years following introduction, by facilitating the rapid increase in prevalence and intensity of A. crassus infection that typically occurs during this time.