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Integrative and Comparative Biology
Integrative and Comparative Biology, volume 54, number 2, pp. 93–100
doi:10.1093/icb/icu028
Society for Integrative and Comparative Biology
SYMPOSIUM
Parasitic Manipulation of Hosts’ Phenotype, or How to Make a
Zombie—An Introduction to the Symposium
Kelly Weinersmith1,* and Zen Faulkes†
*Graduate Group in Ecology, University of California Davis, 1005 Wickson Hall, Davis, CA 95616, USA; †Department of
Biology, The University of Texas-Pan American, 1201 W. University Drive, Edinburg, TX 78539, USA
From the symposium ‘‘Parasitic Manipulation of Host Phenotype, or How to Make a Zombie’’ presented at the annual
meeting of the Society for Integrative and Comparative Biology, January 3–7, 2014 at Austin, Texas.
1
E-mail: [email protected]
Synopsis Nearly all animals in nature are infected by at least one parasite, and many of those parasites can significantly
change the phenotype of their hosts, often in ways that increase the parasite’s likelihood of transmission. Hosts’ phenotypic changes are multidimensional, and manipulated traits include behavior, neurotransmission, coloration, morphology, and hormone levels. The field of parasitic manipulation of hosts’ phenotype has now accrued many examples of
systems where parasites manipulate the phenotypes of their hosts and focus has shifted to answering three main questions. First, through what mechanisms do parasites manipulate the hosts’ phenotype? Parasites often induce changes in
the hosts’ phenotypes that neuroscientists are unable to recreate under laboratory conditions, suggesting that parasites
may have much to teach us about links between the brain, immune system, and the expression of phenotype. Second,
what are the ecological implications of phenotypic manipulation? Manipulated hosts are often abundant, and changes in
their phenotype may have important population, community, and ecosystem-level implications. Finally, how did parasitic
manipulation of hosts’ phenotype evolve? The selective pressures faced by parasites are extremely complex, often with
multiple hosts that are actively resisting infection, both in physiological and evolutionary time-scales. Here, we provide an
overview of how the work presented in this special issue contributes to tackling these three main questions. Studies on
parasites’ manipulation of their hosts’ phenotype are undertaken largely by parasitologists, and a major goal of this
symposium is to recruit researchers from other fields to the study of these phenomena. Our ability to answer the three
questions outlined above would be greatly enhanced by participation from individuals trained in the fields of, for
example, neurobiology, physiology, immunology, ecology, evolutionary biology, and invertebrate biology. Conversely,
because parasites that alter their hosts’ phenotype are widespread, these fields will benefit from such study.
Introduction
Nearly all animals are infected by parasites, and
many parasites exert profound influences on the
phenotype of their hosts (Moore 2002; Hughes
et al. 2012). However, the influence of parasites is
often unnoticed by researchers. Ethologists and
neuroscientists, for example, rarely look for, or
consider how, infections might change the phenotype
of the organisms they are studying. While not all
parasites alter their hosts’ phenotype (e.g., Joseph
and Faulkes 2014) nor are all traits of the host influenced by manipulative parasites, it is important to at
least understand which parasites infect a focal host
species and consider how the parasite may influence
the trait in question. An ecologically and evolutionarily relevant understanding of hosts’ phenotype
requires understanding how parasites influence it,
and studying parasites may uncover previously unexplored links between the brain, immune system, and
behavior.
Infection results in changes to the phenotype of
the host through one of three main routes: (1) infection induces pathology that may or may not benefit
the parasite; (2) the host induces adaptive changes in
its phenotype in ways that reduce the costs of infection, or that eliminates the parasite; and (3) parasites
may adaptively manipulate the phenotype of their
host in ways that increase the probability of transmission (Poulin 2010). The category into which a
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94
parasite-associated change in phenotype should
fall is not always obvious. For example, Paranjpe
et al. (2014) found that side-blotched lizards
(Uta stansburiana) infected with the apicomplexans
Plasmodium mexicanum or Schellackia sp. thermoregulated at lower than preferred body temperatures
and exhibited greater variability in body temperature
relative to uninfected individuals, in contrast to some
reptiles that respond to infections by increasing body
temperatures via ‘‘behavioral fever’’ (Kluger 1979;
Firth and Turner 1982; Monagas and Gatten 1983).
This result could arise if pathology prohibits lizards
from achieving their preferred thermal level, if the
hosts adaptively combat the infection by reducing
their body temperature, or because of the parasite’s
manipulation if an inability to maintain optimal
body temperatures makes the lizards more hospitable
hosts for the parasites, or more likely to be bitten by
the appropriate vector of the parasite. Alternatively,
lizards that maintain lower or more variable body
temperatures may be more susceptible to infection.
Careful study and controlled infections are often required to confirm that the change in host phenotype
arose post-infection, and to determine through
which of the three routes, in which combinations,
phenotypic changes were induced. While the manuscripts in this special issue deal mainly with cases in
which parasites manipulate the host’s phenotype,
ecologically and evolutionarily important phenotypic
changes arise through the other routes as well (e.g.,
Boze and Moore 2014). Concerns about which category is associated with particular changes in the
host’s phenotype may cause us to under-appreciate
the population, community, and ecosystem-level implications of those changes. The focus should go
beyond categorizing parasite-associated changes in
phenotype of the host and should instead focus on
how these categories differ in their effects on the
evolution of phenotype, and what they can tell us
about links between the brain, immune system, and
behavior.
Our goal for this symposium was to expose a
broad range of biologists to the field of phenotypic
manipulation of hosts’ phenotypes, in the hope of
recruiting a greater diversity of scientists to tackle
emerging questions in this field. Our symposium focused on these emerging questions: (1) through what
mechanisms do parasites manipulate hosts’ phenotypes? (2) What are the ecological implications of
manipulation? (3) What are the evolutionary implications of infection? Decades of research, conducted
mainly by parasitologists, reveal many cases of parasitic manipulation (Moore 2002, 2012; Hughes et al.
2012), and many questions about parasites will only
K. Weinersmith and Z. Faulkes
be answered by multi-pronged investigations from
scientists with a diverse set of skills. For example,
understanding the mechanisms through which parasites induce changes in hosts’ phenotypes will require
immunologists, neurobiologists, scientists familiar
with ‘‘-omics’’ techniques, and bioinformaticians.
Quantifying the ecological and evolutionary
implications of parasite-induced changes in hosts’
phenotypes will be forwarded by collaboration
among parasitologists, ecologists, evolutionary biologists, and neurobiologists. Below we discuss how
participants in the symposium are addressing the
three questions posed above, and discuss how an
integrative approach to these questions will benefit
the study of parasitic manipulation of phenotype
while benefiting other fields as well.
Mechanisms of manipulation: How do
parasites manipulate hosts’ phenotypes?
Parasites are capable of inducing phenotypic changes
in their hosts that are both multidimensional and
extremely specific (Cezilly and Perrot-Minnot 2010;
Thomas et al. 2010; Cézilly et al. 2013). One of the
best known examples is the protozoan parasite
Toxoplasma gondii, which infects cats (Felidae) as
definitive hosts (i.e., the hosts in which sexual reproduction occurs), but practically any species of warmblooded animals can serve as an intermediate host
(Dubey 2010). In rodents, infection by T. gondii is
associated with decreased learning and memory, increased activity, increased time spent in the open,
and reduced neophobia (Webster 2007), but the
most dramatic consequence of infection is a change
in the rats’ responses to the smell of cats’ urine.
Uninfected rats avoid the smell of predators’ urine,
including cats, but infected rats lose their aversion to
the smell of their feline predators; in some cases, rats
are attracted to this scent (Berdoy et al. 2000; Vyas
et al. 2007; Lamberton et al. 2008). Infected rats still
avoid the smell of urine from non-feline predators,
showing the specificity of the change. The rats’ fearlessness likely increases the probability of contact
with feline predators, which is predicted to increase
the probability of T. gondii infecting its definitive
host. Kaushik et al. (2014) found that rats infected
with T. gondii prefer the smell of urine from wild
cats (cheetahs and pumas) over that from domestic
cats, which may be explained by wild cats being
more suitable definitive hosts or by a longer coevolutionary history between wild cats and T. gondii.
This alteration in rats’ behavior appears to involve
long-lasting (Ingram et al. 2013) changes in the
limbic system (House et al. 2011; Mitra et al.
Zombie symposium introduction
2013), but neuroscientists cannot recreate this
manipulated phenotype in the laboratory. Hostmanipulating parasites can be thought of as ‘‘evolutionary neuroscientists’’ (Adamo 2013; Cézilly et al.
2013; Maure et al. 2013), and understanding how
parasites manipulate their host’s phenotype will
teach us about links between the brain, behavior,
and immune system (Helluy 2013; Holland and
Hamilton 2013; Libersat and Gal 2013; McCusker
and Kelley 2013).
Neurobiologists often see animal behavior as the
output of the nervous system, so it is a reasonable
hypothesis that parasites would manipulate their
hosts by affecting the nervous system. A secondary
hypothesis is that the more precise the manipulation,
the more likely it is to involve the nervous system.
Nervous system output is usually described as being
determined by electrical signals within and chemical
signals between neurons, and neurobiologists have
traditionally leaned more heavily on using electrophysiological techniques to control neurons, and
thus behavior. In contrast, there are few documented
cases of a parasite affecting its host by generating or
altering electrical signals directly, but there are many
cases of parasites controlling their host’s behavior by
exploiting chemical signals (Lafferty and Shaw 2013).
Jewel wasps’ manipulation of their cockroach host,
detailed by Libersat and Gal (2014), is one of the
best examples of how a nervous system can be hijacked by another animal using a cocktail of neuroactive chemicals. ‘‘Parasite’’ usually conjures the
image of small animals living partly or entirely
within the body of a host for most of its life cycle,
but parasitoids, like the jewel wasp, are free-living as
adults, but lay eggs within a host. Adult jewel wasps
manipulate the host in ways that benefit their offspring. Like many parasites, the parasitoid jewel wasp
uses neuroactive chemicals that alters the host’s behavior and delivers them by precise and sudden injection of venom. The venom specifically impairs the
initiation of voluntary walking in the stung roach,
but not other locomotor behaviors, such as escape
responses. The cocktails of venom achieve this
through the dopaminergic system in the subesophageal ganglion, and almost certainly the brain (supraesophageal ganglion), although research on the latter
is not as advanced. Other venoms can be extremely
variable (Sunagar et al. 2014), so studying other
parasitoid systems is likely to yield entirely new
mechanisms
of
manipulation
by
venom.
Undoubtedly, the success of the jewel-wasp research
program lies in part with the fact that cockroaches
were intensively studied as subjects for neuroethology, e.g., walking (Ritzmann 1993; Zill 2010), escape
95
(Camhi 1984; Camhi and Levy 1988), and memory
(Mizunami et al. 1998), including the locomotor
behaviors manipulated by the jewel wasp. This
provided a foundation upon which the investigation
of manipulation could be investigated.
Like cockroaches, decapod crustaceans have been
stalwart model organisms in neuroethology for
decades (Wiese 2002a, b), which makes crustaceanparasite systems promising models of understanding
the mechanisms of parasitic manipulation. Carreon
et al. (2011) and Carreon and Faulkes (2014) examined larval tapeworms infecting the nervous system
of shrimp. Because the parasites infect the nervous
system, they are in an excellent position to manipulate the host, but this risks disrupting the fine connections between neurons needed for basic
functioning. Carreon and Faulkes (2014) hypothesized that parasites living in the nervous system
will be distributed non-randomly, perhaps due to
the trade-off between control and damage. The
larval tapeworms in shrimp appear to fall somewhere
between the two extremes. They hypothesize that the
position of parasites in the nervous system can suggest whether parasites use targeted (scalpel) or nonspecific (shotgun) tactics to affect their hosts’
behavior.
Parasites’ ability to infect, and presumably manipulate, the nervous system, has a trade-off over
evolutionary timeframes as well as physiological or
organismal scales, as Fredensborg (2014) shows.
Helminth parasites that infect the nervous system
are limited to a much narrower range of hosts
than those helminths that infect other types of
tissue, but have larger, more specific effects. Those
that infect tissues such as muscle can infect a wider
variety of hosts, but the level of manipulation is
much less specific. That is, parasites that infect nervous systems might alter higher level behaviors, such
as microhabitat choice, while those infecting muscle
might induce general lethargy. Across a wider range
of parasitic taxa, the location of infection, and the
type of host correlates with the mechanisms of manipulation (Lafferty and Shaw 2013).
Another way in which parasites manipulate host’s
phenotypes relies less on altering neurons in the nervous system, and more on interfering with connections between the host’s immune and nervous
systems (e.g., Helluy 2013; Holland and Hamilton
2013; McCusker and Kelley 2013). Adamo (2014)
discusses ways in which sexually transmitted infections (STIs) may exploit immune/neural communication signals that increase the probability of
transmission to another host. Infected hosts frequently are avoided by conspecifics, considered less
96
attractive mates, and initiate sickness behaviors that
divert energy away from reproduction and toward
immune-system functioning. All of these scenarios
result in fewer opportunities for transmission for
the STI, and thus in some cases selection should
act on STIs to mask signs of infection in their host
and reduce hosts’ sickness behavior. A final behavioral response to infection by hosts is terminal reproductive investment, putting as much energy as
possible into reproduction when future reproductive
prospects are dim (e.g., because infection will eventually result in the host’s death). This final behavioral
defense may benefit both host and parasite, as it increases fitness of the host given current circumstances and exposes parasites to more potential
hosts. These behavioral changes are likely achieved
through interactions with the immune and nervous
systems and may have important implications for
theories of sexual selection, provide important insights for the field of psychoneuroimmunology, and
provide practical benefits (e.g., allowing us to suppress sickness behavior and sexual dysfunction).
While many studies have focused on measuring
one or a few potential mechanisms at a time, the
rise of ‘‘-omics’’ techniques allows us to focus on
candidate mechanisms while casting a wide net to
capture other mechanisms as well (Biron and
Loxdale 2013; Hughes 2013; Hébert and AubinHorth 2014). de Bekker et al. (2013) use metabolomics to understand manipulation of ants by fungal
parasites, and de Bekker et al. (2014) discuss the
importance of controlled infections and controlling
for heterogeneity when employing ‘‘-omics’’ techniques. These authors highlight the sensitivity of
the transcriptome, metabolome, and proteome to
abiotic factors such as time of day, temperature,
and humidity and biotic factors (e.g., parasite dose,
interactions with conspecifics), and stress the importance of laboratory infections to control for these
factors. Removing noise associated with these factors
will be crucial for acquiring high-quality data and
honing in on mechanisms of manipulation. As
these papers show, parasites can alter neural, hormonal, immune, and/or molecular physiology
through a wide array of mechanisms. There are surprisingly few systems in which parasitic infection (or,
in the case of parasitoids, attack) on hosts can be
controlled rigorously, and in which the necessary
baseline knowledge of the hosts’ physiology and behavior is present. Thus, understanding the mechanisms of parasitic manipulation remains a
challenging field, but one ripe for further study
and begging for an integrative approach.
K. Weinersmith and Z. Faulkes
What are the ecological implications of
parasites changing their host’s
phenotype?
While individual parasites may be small and difficult
to see, the combined biomass of parasites in an
ecosystem can exceed the biomass of top predators
(Kuris et al. 2008). In addition to accounting for an
important proportion of the biomass in an
ecosystem, the biomass of hijacked hosts can
sometimes exceed the biomass of uninfected hosts
within a species (Kuris et al. 2008). Phenotypemanipulating parasites can have important impacts
on, for example, the dynamics of food webs,
apparent
competition,
and
biodiversity
of
ecosystems, yet ecological implications of manipulating parasites have been studied in few systems and
effects are often hypothesized but not quantified
(Léfevre et al. 2008; Lafferty and Kuris 2012;
Mescher 2012). Not all parasites manipulate their
hosts in the strict sense (i.e., changes in the host
increase the fitness of the parasite, and are therefore
adaptive for the parasite), and both adaptive and
non-adaptive changes have important biological
consequences.
Parasites that manipulate their host’s phenotype
are likely to have important ecological implications
when they exert dramatic changes, infect a large proportion of the host population, or when they infect
abundant or ecologically important hosts (Lafferty
and Kuris 2012). The nematode Physocephalus sexalatus infects an ecosystem engineer, Phanaeus dung
beetles, and impacts behaviors that define this insect
as an ecosystem engineer (Boze and Moore 2014).
Infected dung beetles eat half as much feces as uninfected conspecifics, which lowers the rate at which
nutrients are returned to the soil and increases the
risk of parasitic infection for other organisms in the
ecosystem. Parasites produce eggs that pass with the
host’s feces back into the environment, and many of
these eggs are killed and thus removed from the environment when ingested by dung beetles (Miller
1961). Additionally, infected dung beetles dig shallower tunnels in which to bury feces, and so infected
individuals contribute less to the aeration and fertility of the soil. However, infection is not associated
with changes in the behavior classically associated
with increased risk of transmission (i.e., increased
risk of predation). Instead, the anorexia observed
in infected dung beetles may well be part of sickness
behavior and may enhance the dung beetle’s defense
against parasites. While this example likely does not
count as ‘‘parasitic manipulation’’ as the behavioral
changes do not clearly benefit the parasite, the effects
97
Zombie symposium introduction
of the modification of the host’s phenotype on the
ecosystem are clear.
From the point of view of a small parasite, the
internal milieu of their host is a complete ecosystem
in its own right, containing diverse habitats (differing
tissues) and potentially several other parasitic species.
Thus, understanding interactions between parasites
in their hosts is crucial for understanding the parasite’s population and community ecology. For example, competition between parasites within a host can
constrain parasites’ sizes and reduce the parasite’s
fecundity (e.g., Brown et al. 2003; Fredensborg and
Poulin 2005). Exploring the host’s dynamics is particularly interesting when the interests of hosts and
manipulating parasites align, as manipulation is believed to be costly and parasites may share the cost
of infection (Poulin 1994, 2010). Weinersmith et al.
(2014) looked for signs of density dependence in two
manipulating trematode parasites of the California
killifish (Fundulus parvipinnis), the most abundant
fish species in southern Californian and Baja
Californian estuaries (Allen et al. 2006; Hechinger
et al. 2007). Euhaplorchis californiensis and Renicola
buchanani infect killifish and induce conspicuous
behaviors that increase the risk of infection by the
parasites’ shared definitive host, predatory birds
(Lafferty and Morris 1996). While other studies
have observed negative density dependence in behavior-manipulating parasites (i.e., a decrease in the
parasite’s size as its intensity or density increased
in the host) (Brown et al. 2003; Dianne et al.
2012), Weinersmith and colleagues observed no density dependence for R. buchanani and there was positive density dependence for E. californiensis. Two
major differences between previous studies and this
study of killifish are that the parasites infecting
killifish are small relative to their host (and are therefore less likely to experience limitation of resources);
the magnitude of the expression of the manipulated
phenotype increases with increasing density of parasites in killifish. Euhaplorchis californiensis may have
been able to achieve a larger size in the presence of
conspecifics by investing less in manipulation at high
densities. Controlled infections are needed, but this
study suggests that within-host dynamics do not
limit the population dynamics of E. californiensis and
R. buchanani, and that positive density dependence
may help to explain why E. californiensis is the most
abundant trematode parasite in the estuaries where it is
found (Hechinger et al. 2007). While many studies in
this field end with speculations about the implications
of parasitic infection, direct or indirect ecological
effects are typically not quantified. Indeed, as Hughes
(2014) notes, even though there are cases that now
appear to be dramatic, textbook examples of parasitic
manipulation were often unseen or not verified for
long periods of time. We have much yet to learn
about this phenomenon.
How did manipulation of the host’s
phenotype evolve?
Parasitic manipulations of hosts are among the most
complex adaptive traits in the organic world (Hughes
2014). Teasing apart the origin of complex traits, like
parasitic alterations of host’s phenotype, is still
difficult for evolutionary biologists, and is typically
considered on a case-by-case basis. Parasitic manipulation is apparently rare across parasites, perhaps
because the transition from one peak in the fitness
landscape to another is challenging. The study of the
evolution of parasitism is made even more complicated because it often requires understanding the
evolutionary history and phylogeny both of parasites
and their hosts, as well as a thorough quantification
of parasites’ extended phenotype. Controlling the
phenotype of another organism requires that parasites adapt to, and thus specialize in, particular host
species. Fredensborg (2014) explores how the type of
manipulation a parasite uses constrains the diversity
of hosts it is able to infect. A previous analysis found
the location of infection and the type of host to be
associated with the type of manipulation a parasite
induced (Lafferty and Shaw 2013). Parasites infecting
invertebrates or the host’s body cavity tend to manipulate the host in ways that increase contact rates
of the host with its predators, while parasites infecting vertebrates or hosts’ muscles, central nervous
system, and some other sites impair the host’s
response to predators (Lafferty and Shaw 2013).
Fredensborg (2014) built upon this analysis and
found that parasites that infect the central nervous
system and/or manipulate the host’s neuromodulation are more constrained in the diversity of hosts
they can infect (i.e., they are constrained to infect
hosts that are more closely related to each other)
relative to parasites that reside elsewhere or rely on
debilitation of the host to increase transmission.
Residing in the central nervous system or manipulating neuromodulation forces manipulating parasites
to be specialists, while residing elsewhere or depending upon debilitation to increase transmission rates
allows parasites to adopt a more generalist strategy
(Fredensborg 2014).
Mauck et al. (2014) explores questions about local
adaptation of Cucumber mosiac virus (CMV), a pathogen of plants that is transmitted between hosts by
aphids. Two virus isolates displayed increased
98
infectivity and higher titers of virus when infecting a
native host relative to a novel one. They also found
that one virus isolate manipulated the phenotype of
the host plant and vector (aphids) in ways likely to
increase transmission when infecting a native host
plant, while transfer to a novel host plant resulted
in changes in the host’s phenotype that likely reduced
transmission of the virus. The second virus isolate
showed non-significant trends toward manipulating
its native host and vector in ways that increased
transmission, but the virus’s ability to manipulate a
non-native host could not be explored because this
isolate was rarely able to infect a novel host plant.
Mauck et al. (2014) highlight the importance of considering genetic differences in the ability of a parasite’s or pathogen’s (in this case, isolate’s) ability to
manipulate the host’s phenotype, and of the importance of local adaptation in the success of manipulation. This is not only important for our
understanding of the evolution of manipulation,
but also for applied purposes and for laboratory
studies of manipulation. For example, understanding
genetic differences and the importance of local adaptation would be important when considering the
efficacy of using a parasite or pathogen to control
an invasive plant or pest. Additionally, in laboratory
studies, it is often more feasible to collect and infect
wild hosts from populations that do not co-occur
with the parasite rather than to establish breeding
colonies using hosts with an evolutionary history
with the parasite of interest. However, if the parasite
is locally adapted to the host population, then
laboratory-breeding may be necessary in order to
accurately quantify the parasite’s manipulation of
the host’s phenotype and to understand the ecological implications of infection.
Conclusions
Interest in manipulative parasites has been rising
over the past decades (Moore 2012), and many documented cases of parasites’ manipulations of hosts’
phenotype now await study by integrative teams of
scientists to elucidate how those manipulations
occur, their ecological importance, and how manipulation evolved in that system. These integrative collaborations would be mutually beneficial. Through
natural selection manipulative parasites have
‘‘learned’’ how to exploit the nervous and immune
systems of their hosts to induce precise changes in
the host’s phenotype. Neurobiologists, physiologists,
and immunologists can hasten their understanding
of links between these systems and the expression
of phenotype in the host, and may discover
K. Weinersmith and Z. Faulkes
previously unexplored connections fruitful for further study. For behavioral ecologists, studying
behavior-manipulating parasites can help explain behavioral variation, average values of traits, expression
of suboptimal behaviors, and correlations between
behavioral traits. For ecologists, incorporating manipulative parasites will help to explain the flow of
energy through food webs (e.g., if parasites make
their hosts easier for predators to catch) and the
distribution of animals in an environment (e.g., if
manipulated hosts exhibit different microhabitat
choice). Parasites that manipulate their host’s phenotype increase or decrease the variability in phenotypic traits on which natural selection can act, and
may be of interest to evolutionary biologists tracking
the trajectory of phenotypic traits across evolutionary
time. We hope that in showcasing the host–parasite
systems discussed above, we can encourage a wider
array of researchers to examine the effects of parasites in organisms with which they are familiar, but
for which they previously have not considered the
impact of parasitic infections.
In this article, we have pointed out several desiderata for the study of parasitic manipulation. First,
that the prevalence and abundance of parasitic infection in the wild are characterized (e.g., Joseph and
Faulkes 2014; Paranjpe et al. 2014). Second, that the
physiology (Carreon and Faulkes 2014; Libersat and
Gal 2014), phylogeny (Fredensborg 2014; Hughes
2014; Mauck et al. 2014), and ecology (Boze and
Moore 2014) of the host are well understood.
Third, that hosts and parasites can be housed and
infected under controlled conditions (de Bekker et al.
2014; Libersat and Gal 2014; Mauck et al. 2014).
Currently, there are very few host–parasite systems
that check even half of these items off the list. This
is not surprising, given the wide range of skills
needed to accomplish even a few of these. We
hope that in showcasing these host–parasite systems,
we can encourage a wider array of researchers to
examine the effects of parasites in organisms with
which they may not be familiar, or for which they
may not have previously considered the impact of
parasitic infections.
Acknowledgments
We wish to thank Jon Harrison, Lori Strong, the rest
of the organizers of the 2014 SICB conference, and
the ICB editorial team for their help organizing the
symposium and this special issue. We thank Janice
Moore and Brian Fredensborg for helpful comments
on an earlier draft of this manuscript. We dedicate
Zombie symposium introduction
this paper to Ada Marie Weinersmith, who was delivered the same week as this paper.
Funding
This symposium was supported by the National
Science Foundation Division of Integrative
Organismal Systems [grant number #1338574]; the
American Microscopical Society; and the Society
for Integrative and Comparative Biology (Division
of Animal Behavior, Division of Invertebrate
Biology, and Division of Neurobiology). K.L.W.
was supposed by block grants from the Graduate
Group in Ecology at the University of California
Davis.
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