Trends in Parasitology
Volume 25, Issue 12, December 2009, Pages 564-572
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Review
Parasitic castration: the evolution and ecology of body snatchers

https://doi.org/10.1016/j.pt.2009.09.003Get rights and content

Castration is a response to the tradeoff between consumption and longevity faced by parasites. Common parasitic castrators include larval trematodes in snails, and isopod and barnacle parasites of crustaceans. The infected host (with its many unique properties) is the extended phenotype of the parasitic castrator. Because an individual parasitic castrator can usurp all the reproductive energy from a host, and that energy is limited, intra- and interspecific competition among castrators is generally intense. These parasites can be abundant and can substantially depress host density. Host populations subject to high rates of parasitic castration appear to respond by maturing more rapidly.

Section snippets

The virulence tradeoff

In the classic Aesop's fable, a couple were fortunate enough to have a goose that laid a golden egg daily. Greed set in and, imagining the goose to be filled with gold, they slaughtered it, only to find its innards like any other goose. Parasites must heed the moral of this fable: those who take too much risk losing everything. A parasite eats a fraction of its host – how much to consume leads to the classic virulence tradeoff 1, 2. Parasite growth and reproduction should increase with parasite

What is a parasitic castrator?

Parasites in many taxa can override the allocation strategy of the host by directing their ‘take’ of host energy solely to host reproductive energy, thereby avoiding a decrease in host viability 3, 4. Some models suggest that such a parasite should take all the reproductive energy of the host, if possible 5, 6, 7, a strategy that castrates the host. Formally defined, parasitic castration is an infectious strategy that requires the eventual intensity-independent elimination of host reproduction

Castration in context

Fecundity reduction or suspension can be a host strategy difficult to distinguish from parasitic castration. For example, theoretically, if hosts can expect to outlive an infection, they might temporarily divert reproductive energy into defense to tackle the infection more effectively 2, 10, 11. Also, there might be some conditions such that a host should respond to infection by partially reducing fecundity even if the infection is permanent 5, 11. Such host adaptations do not constitute

What do parasitic castrators take from their hosts?

The energetics of reproduction is not simply the mass of the gonads (generally 5–15% of the mass of the host). The host puts mass into the associated structures (e.g. sperm ducts, seminal receptacles and vitelline glands), secondary sexual characteristics (e.g. copulatory organs, ornaments and bright colors) and packaging material for offspring (e.g. egg shells). In addition, substantial behavioral and metabolic energy goes into activities such as mate selection, choice of oviposition sites,

Are parasitic castrators important?

Although unfamiliar to medical and veterinary parasitology, castration is common among parasites of fishes and invertebrates (Table 1) 1, 8, 9, 10, 11. For instance, in three estuaries along the coast of southern California and Baja California, parasitic castrators comprised 20% of the 150 detectable species of infectious agents [21]. The pooled biomass of parasitic castrators was 3–11 kg/ha, which exceeded the biomass of the macroparasites by two orders of magnitude. The biomass of parasitic

The extended phenotype

Parasitized hosts present a complex extended phenotype [24] (which sometimes differs considerably from an uninfected host phenotype, even if they visually appear identical) that attempts to express two genotypes: host and parasite [9]. Parasitic castration resolves this internal conflict because the residual fitness of the host is reduced to zero, and its morphology, behavior and physiology now simply supply the reproductive success of the castrator by functioning as its extended phenotype [2].

How is parasitic castration achieved?

Though castration is often achieved through the selective targeting of reproductive energy, castration can also simply be the consequence of a nutritional drain, and hosts might be programmed to make up for the energetic loss by first sacrificing reproduction [11]. The energy drain hypothesis fits some bopyrid isopods that parasitize certain shrimps and crabs. Castration could also target host reproductive energy by consuming gonads [7] or by indirectly manipulating the optimal resource

Ecological and evolutionary consequences

Parasitic worms are often aggregated, meaning that, for a given level of infection, more hosts are uninfected or are heavily infected than would randomly be expected. Highly aggregated distributions of parasites among hosts are so often reported that this dispersion pattern is almost axiomatic for macroparasites [34]. In marked contrast, dispersion of individual parasitic castrators (or a mated pair) often approaches a uniform distribution with a distinct mode and mean of one parasite per

Concluding remarks

The parasitic strategy of castration is a unique interaction between consumer and resource. Parasitic castration is a response to the classic virulence tradeoff between consumption and longevity. The most commonly observed castrators are larval trematodes in snails and isopod and barnacle parasites of crustaceans, though many other taxonomic groups have independently adopted the strategy. Invertebrates and small fishes appear to be the primary hosts for parasitic castrators because a

Acknowledgements

Rachel Fogelman and Ryan Hechinger provided comments on the manuscript. Funding was provided by the National Science Foundation/National Institutes of Health Ecology of Infectious Diseases Program (DEB-0224565).

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