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PARASITE MANIPULATION: CASTRATION
JESSICA FREDERICKS
Ecology of Animal Parasites
Dr. Gwyneth Jones
Monday, April 12th, 2010
INTRODUCTION
Parasitic castration is considered a manipulation of the host and is defined as “an infectious
strategy that requires the eventual intensity-independent elimination of the host reproduction as
the primary means of acquiring energy” (Lafferty & Kuris, 2002). Mechanisms can be direct or
indirect modification to reproduction and specifically to the use of the gonads. To achieve
castration of a host a parasite can use mechanical, hormonal, nutrient withdrawals or genetic
modification methods. Parasitic castrators can manipulate a host’s secondary sex characteristics,
organs, secretions, growth, and behavior and can even lead to permanent sterility or sex reversal
of the host. Parasitic castrators are able to eliminate the amount of energy being used by the host
as reproductive effort. Reproductive effort is tradeoff of energy from the host to create offspring
and increase its inclusive fitness. The parasitic castrators are able to redirect this energy to serve
their own to fitness will still maintaining a relatively healthy host.
The most common examples of parasitic castrators include larval trematodes in snails and
isopods and barnacles in crustaceans (Lafferty & Kuris, 2009). A table of taxa falling into the
parasitic castrator group can be found in Figure 1. Organisms that are not considered parasitic
castrators include: taxa that only partially reduce fecundity, taxa that use pathogens to induce
castration or macroparasites that cause castration only due to varying intensity in
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Figure 1: Examples of parasitic castrator taxa and their hosts; also including remarks on specified
taxa (Lafferty & Kuris, 2009)
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their host (Lafferty & Kuris, 2009). Parasitic castrators are generally host specific and have a
uniform distribution in host populations. Often only one adult and its immediate offspring
occupy an individual host (Fogelman, Kuris, & Grutter, 2009). Length of time spent in one host
is generally quite long for a parasitic castrator, possibly due to its need to grow to its large size.
Generally, parasitic castrators range from 3-30% of their host’s mass; this size relationship
between host and parasite can be seen in Figure 2. showing parasitic castrator isopod size in
relation to their fish hosts (Fogelman, Kuris, & Grutter, 2009). Parasitic castrators appear to be
successful adaptive manipulators of their hosts to increase their fitness by improving
environment through castration.
Figure 2: Correlation between fish weight and its isopod parasite weight showing a larger host is
able to grow larger parasitic castrators. Also showing the larger size of parasitic castrators in
comparison to their host (Fogelman, Kuris, & Grutter, 2009).
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DISCUSSION
Effects on host
Effects of parasitic castration vary considerably by host, especially due to host sex differences,
but the type of effects of different parasitic castrators are able to inhibit or modify hosts by their
secondary sex characteristics, organs, secretions, growth, and behavior and can lead to
permanent sterility or perhaps even sex reversal of the host. Most commonly thought of results of
parasitic castration are effects to secondary sex characteristics. Secondary sex characteristics are
not direct apart of the reproductive system but when altered they normally lead to juvenilization
of the host. This juvenilization is characterized by a reduction in the size of characters that are
involved in mating, competition for mates and providing for offspring. Also included in
secondary sex characteristic effects is the habitation of a parasitic castrator in the egg sac in some
crabs, sacculination, a castration strategy of the sacculinid crustacean (Hartnoll, 1962). Effects to
the host’s reproductive organs are what define parasitic castrators. Parasite’s may only reduce the
size of the gonads, destroy parts of the gonads, or even total atrophy of these organs. Parasitic
castrators normally do not only deteriorate the reproductive organs, but also other organs in the
host as well, at varying degrees. The parasites may have effects on many organs in the host body
(eg. metacercariae), focus on the gonads or have only little effect on the gonads but is correlated
with reduced gonads (Baudoin, 1975). Secretions in the host body, such as lipids and hormones,
are also effected by parasitic castrators. Reduced energy for reproduction, due to castration, may
lead the host to produce greater quantities of lipids in its internal fluids or create fat depositions.
Hormones in the host can be modified by the parasite as a result of endocrine organs destruction
or the addition of hormones secreted by the parasite leading to reduced reproduction in the host.
A trait often associated with hosts parasitized with parasitic castrators is abnormal growth, more
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specifically gigantism. In many host species there is a positive correlation between an increase in
size and their parasitic castration. One example of this is the host snail, Lymnaea truncatula,
parasitized by the larval stage of Fasciola hepatica where the weight of the infected snails can be
twice that of an uninfected snail after the same growth period (Figure 4), following parasitic
castration, which is shown by the cessation of egg production visible in Figure 5 (Wilson &
Denison, 1980). This growth may also be related to an observed increase in host viability.
Another possibility for increased host viability could be related to the apparent lack of
pathological conditions in host parasitized by castrators. Sexual and parental behaviors can also
be altered in parasitic castrator hosts. An example of a behavior change in a host due to parasitic
castration can be found in parasitized shore crabs which keep a distance from shallow water
mating locations by remaining in deep water (Rasmussen, 1959). Other behavioral changes
include decrease in mate attracting and searching, decrease in aggressive behaviors related to
mate competition and a lack of parental care. A summary of some effects to castrated parasitized
hosts, including the results of growth, reproduction and energy levels, can be found in Figure 5;
this also compares the castration strategy to a typical consumer parasite strategy.
Mechanisms
Mechanisms of parasitic castration can be direct or indirect forms resulting in a reduction of the
the reproduction of the host and an increase in available energy for the parasite (Lafferty & Kuris,
2009). Mechanisms of castration can be mechanical, hormonal, nutrient withdrawals or genetic
modification and normally require high host specificity of the parasite. Direct mechanisms are
mechanical damage to gonads and other important organs that could be included in reproduction
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Figure 3: Dry weight of Lymnaea truncatula snails over time (days) in the control and Fasciola
hepatica infected snails (Wilson & Denison, 1980)
Figure 4: Eggs laid of Lymnaea truncatula snails over time (days) in the control and Fasciola
hepatica infected snails (Wilson & Denison, 1980).
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Figure 5: Comparison of body size, available energy, reproduction and volume of parasites over
time (days) in an uninfected host, a host parasitized by a consumer, and a host parasitized by a
castrator. In the parasitized hosts the thresholds for the cessation of growth feeding and
reproduction are also drawn (Hall, Becker, & Ca´ceres, 2007).
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by partial or complete ingestion. Larval trematodes are an example of this direct mechanism;
they ingest gonad tissue to castrate their molluscan hosts (Cheung & Synder, 1962). An indirect
mechanism, the withdrawal of nutrients, can be an immediate cause of castration as the host
would look for a way to reclaim the lost energy by cutting its reproductive energy uses. Although,
as previously mentioned, increased growth, lipid concentration and gigantism are also effects to
the host so if the host is able to continue growing the nutrients exploited by the parasite must be
very selective (Baudoin, 1975). Hormones can be released by the parasite, that could be referred
to as “castrating hormones” (Baudoin, 1975), that indirectly change the gonads and their function.
Parasitic castrators can also interrupt the host’s neuroendocrine system using their own hormones
or by modification or destruction of host glands or other neuroendocrine organs. This mechanism
can conflict with the production of hormones needed for reproduction and growth of the gonads,
another mechanism used by larval trematodes (Loker & Adema, 1995). Genetic interference is a
complex indirect mechanism of parasitic castration used by few parasites. Genes to be altered
that might interfere with reproduction would be those genes that could control gonad growth, or
genes in the brain that signal reproduction. An example of this type of parasitic castration
mechanism was studied in the brain of host mollusc Haliotis asinine, comparing neuropeptide
genes in the brain, related to seasonal mating in molluscs, parasitized by digenian trematode
Allopodocotyle species and uninfected individuals by season. Results of this study showed the
expressions of these genes were altered in the brain of the host by the parasite to simulate actions
of the mollusc during non-mating seasons to eliminate reproduction in the host (Rice, McGraw,
O'Brien, Reverter, Jackson, & Degnan, 2006). A parasitic castrator is able to use any or many of
these mechanisms to castrate its host to eliminate its use of energy for reproduction so they can
be redirected to sustaining the parasite.
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Parasite benefits
This type of host manipulation, castration by parasites, exists because it provides benefits, an
increase to fitness, for the type of parasites that use it. In general, castration is considered a way
to increase energy available to the parasite without compromising the viability of the host,
thereby providing a location for growth and reproduction for the parasite for an extended time.
When reproduction operations do not use energy in the host, the host is likely to use this energy
to grow, increase its lipid concentration and fat depositions throughout its body. This provides
nutrients useful to the parasite. Types of parasites using these nutrients generally have a high
lipid concentration themselves. Castrating parasites increase a parasitized host viability, which
means a parasitized, castrated host may not be more viable than a non-parasitized host, but is
most likely more viable that a parasitized, non-castrated host (Baudoin, 1975). A castrated host is
subject to less risk and expenditure than a non-castrated host. For example, the host does not
have to engage in dangerous mate or territory competition, search for nest materials or care for
offspring which would subject the host to predation. These are all risks a normally reproducing
host would perform, but due to castration will be more viable and therefore the parasite can
remain in the same host for longer to grow and reproduce. Increase in host size also benefits the
castrating parasite; a larger host can defend against predators more effectively, has more fat
stores for parasite use (Baudoin, 1975). Overall, the castrated host is safer and is a better
resource providing host that increases the fecundity of a parasite that is able to immobilize
reproduction efforts.
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Parasite costs
Not all parasites castrate their hosts and this is because for some parasites, castration costs
outweigh the castration benefits. Costs of parasitic castration include factors of parasite energy
output and host population. Mechanisms of castration that are very energy expensive include
those involving hormones. If a parasite must constantly secrete hormones they create to disrupt
all host physiological feedback mechanisms this will certainly involve a large expenditure of
energy. If the parasite is able to use these secreted hormones in another way to benefit itself then
in this case the energy expenditure may be well worth it (Baudoin, 1975). Creation of structures
to destroy the host gonads can also be a great expenditure of energy in the growth of the parasite.
An obvious appearing disadvantage to castrating individuals in the host species is that this does
not allow for reproduction of host offspring that could potentially be hosts for the parasite’s
offspring. This cost appears as the parasitic castrator decreasing its own species fitness, although
this may be a way to increase individual fitness. Other individual parasites would not be able to
parasitize these hosts and reproduce; therefore the successful parasite can increase its own
genotype frequency in the species population when it reproduces. Intra and interspecific
competition is quite intense for these reasons (Lafferty & Kuris, 2009). For this manipulation
strategy, parasitic castration, to provide increased fecundity in a parasite the benefits must
outweigh these costs.
Evolution of parasitic castrators
Parasitic castrators have two major adaptations that can be discussed from an evolutionary
perspective; castration and its large size within the host. Castration, as an adaptation, evolved for
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the parasites to make greater use of their host by redirecting reproduction effort energy. If the
parasite was able to eliminate reproduction efforts the host would have expendable energy that
could be consumed by the parasite. Size of parasitic castrators is also important in their evolution.
Parasitic castrators may grow so large because they spend a longer time in the host, but also
having only one large parasite within a host is a good evasion strategy against immune response.
Many small parasites inhabiting the same host are more likely to trigger an immune response
than one large parasite. Another pathway of evolution for castration could use this adaptation as
a relief mechanism to save host viability. If the host is under considerable stress from parasitism
from a large parasite it may not live long, but if the parasite can relieve some of the host’s other
stresses, such as reproduction effort, then the host will be able to survive longer to harbor the
parasite and the parasite offspring (Baudoin, 1975).
CONCLUSIONS
Manipulation?
REFERENCES
Baudoin, M. (1975). Host castration as a parasitic strategy. Evolution , 29, 335-352.
Cheung, T. C., & Synder, R. W. (1962). Studies on host-parasite relationships between larval trematodes
and their hosts. I. A review. II. The utilization of the host's glycogen by the intramolluscan larvae of
Glypthelmins pennsylvaniensis Cheng, and associated phenomena. Transactions of the American
Microscopical Society , 81 (3), 209-228.
Fogelman, R. M., Kuris, A. M., & Grutter, A. S. (2009). Parasitic castration of a vertebrate: Effect of the
cymothoid isopod, Anilocra apogonae, on the five-lined cardinalfish, Cheilodipterus quinquelineatus.
International Journal for Parasitology , 39, 577-583.
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Hall, S. R., Becker, C., & Ca´ceres, C. E. (2007). Parasitic castration: a perspective from a model of
dynamic energy budgets. Integrative and Comparative Biology , 47 (2), 295-309.
Hartnoll, R. G. (1962). Parasitic castration of Macropodia longirstris (Fabricus) by a Sacculinid.
Crustaceana , 4, 295-300.
Lafferty, K. D., & Kuris, A. M. (2009). Parasitic castration: the evolution and ecology of body snatchers.
Trends in parasitology , 25 (12), 564-572.
Lafferty, K. D., & Kuris, A. M. (2002). Trophic strategies, animal diversity and body size. Trends in Ecology
and Evolution , 17, 507-513.
Loker, E. S., & Adema, C. M. (1995). Shistosomes, echinostomes and snails: comparative immunobiology.
Parastitology Today , 11, 120-124.
Rasmussen, E. (1959). Behavior of sacculinized shore crabs (Carcinus maenas Pennant). Nature , 183,
479-480.
Rice, T., McGraw, E., O'Brien, E. K., Reverter, A., Jackson, D. J., & Degnan, B. M. (2006). Parasitic
castration by the digenian trematode Allopodocotyle sp. alters gene expression in the brain of the host
mollusc Haliotis asinina. FEBS Letters , 580, 3769-3774.
Wilson, R. A., & Denison, J. (1980). The Parasitic Castration and gigantism of Lymnaea truncatula
infected with the larval stages of Fasciola hepatica. Z. Parasitenkd. , 61, 109-119.