Janice Moore

Parasitic manipulation: where are we and where should we go?

How a parasite (or its offspring) moves from onehost to the next remains a central topic in parasitol-ogy. Understanding such strategies is at the heart ofapplied aspects of parasitology, but it is also im-portant for solving more basic biological questions.One strategy of transmission that is especially in-triguing is that of host manipulation, which occurswhen a parasite enhances its own transmission byaltering host behaviour. We begin this paper witha brief historical overview of the ‘manipulation hy-pothesis,’ in order to illuminate past and present re-search on this transmission strategy, as well as currentchallenges.Scientists were beginning to suspect that parasitescould manipulate their hosts early in the 20th century(e.g. Cram, 1931). In 1952, van Dobben reported thatfish retrieved from cormorants (definitive hosts) werefar more likely to be intermediate hosts of the cestodeLigula intestinalis than were fish captured by fisher-men. Bethel and Holmes (1973, 1977) used labora-tory experiments to show that the cystacanths of theacanthocephalan Polymorphus paradoxus provoke ab-normal behaviours in the amphipod (Gammarus la-custris ; intermediate host), and then verified the re-sulting increased predation risk from ducks (definitivehosts).Since that time, there has been increasing enthusi-asm among parasitologists for the study of phenotypicchanges in parasitised animals. The idea that parasitescould manipulate the phenotype of their host and thusenhance their own transmission became rapidly popu-larnotonlybecauseitwasinherentlyafascinatingphe-nomenon, but also because it offered parasitologists anopportunity to demonstrate the ubiquitous importanceof parasites to a broader community of scientists. Dueto an impressive number of studies performed duringthelastthreedecadesonthistopic,parasite-inducedal-terations of host phenotypes are now documented for awiderangeofparasites(seeBarnardandBehnke,1990;Combes, 1991, 1998; Poulin, 1998; Moore, 2002 forreviews). These studies have demonstrated that a largerange of host phenotypic traits can be altered by para-sites (e.g. behaviour, morphology and/or physiology),and that the alterations can vary greatly in their magni-tude, from slight shifts in the percentage of time spentinperformingagivenactivitytotheproductionofcom-plex and spectacular behaviours (Poulin and Thomas,1999; Moore, 2002).The most popular example of parasitic manipula-tion in ecological textbooks seems to be the trema-tode“brainworm” Dicrocoeliumdendriticum .Ants(in-termediate hosts) infected with this trematode ascendblades of grass, a behaviour that probably enhancestransmission to grazing sheep. However, this is not thebest exemple of parasitic manipulation. As one mightimagine, it is difficult to study ant predation by sheep,and the relative numbers of infected and uninfectedants that are eaten by these herbivores remain a mys-tery. There are however many impressive examples ofapparent host manipulation that are more amenableto quantification. For instance, numerous trophicallytransmitted parasites have been shown to alter the be-haviour of their intermediate hosts in a way that in-creases their vulnerability to predatory definitive hosts(Lafferty,1999;Berdoyetal.,2000;Moore,2002).Par-asites also manipulate host habitat choice; arthropodsharbouring mature nematomorphs or mermithids seekwater and jump into it, thereby allowing the parasiticworm to reach the aquatic environment needed for itsreproduction (Thomas et al., 2002a). Mermithid nema-todes can also feminize male insect behaviour whenparasitetransmissionisdependentonafemale-specificbehaviour (Vance, 1996). Parasitic wasps can maketheir spider host weave a special cocoon-like structuretoprotectthewasppupaeagainstheavyrain(Eberhard,2000, see also Brodeur and Vet, 1994), or can evencause the host to seek protection within curled leavesto protect pupae from hyperparasitoids (Brodeur andMcNeil, 1989). Viruses may stimulate superparasitismbehaviour in solitary parasitoids and thus achieve hor-izontal transmission (Varaldi et al., 2003). Some dige-neans drive their molluscan intermediate hosts towardideal sites for the release of cercariae (Curtis, 1987).‘Enslaver’ fungi make their insect hosts die perchedin a position that favors the dispersal of spores by thewind (Maitland, 1994). Vector-borne parasites can ren-der their vertebrate hosts more attractive to vectors,and/orcanmanipulatethefeedingbehaviourofvectorsto enhance transmission (Hamilton and Hurd, 2002).Allthesespectacularphenotypicchangeshavebeenin-terpreted as the sophisticated products of natural selec-tionthathasfavoredhostmanipulation,thusincreasingthe likelihood that parasite propagules will encounterthe next host or a suitable habitat. From an evolution-ary point of view, these changes are classically seen ascompelling illustrations of the ‘extended phenotype’

Parasite manipulation of host behaviour: should hosts always lose?

Parasites of all kinds alter the behaviour of their hosts. In many systems, these behavioural modifications appear adaptive for the parasite, by facilitating the completion of its life cycle. However, not all parasitized hosts are under the influence of parasites. This may be due to the timing of the onset of behavioural manipulation by the parasites: changes in behaviour may coincide with completed parasite development and only appear late in the infection. In addition, certain hosts may oppose the parasites attempts at manipulating their behaviour. Hosts with high expected future reproductive success, i.e. young hosts or hosts that have not yet reproduced, are more likely to benefit by opposing the influence of parasites, as their expected gains would outweigh the costs of opposition. Such conditional opposition would be a better alternative to resistance to infection itself if resistance is costly, and would explain the considerable variability often observed in the behavioural responses of parasitiaed hosts

The Behavior of Parasitized AnimalsWhen an ant … is not an ant

were a species of social parasite, and he began dissections in preparation for describing the new species. At that point, he realized that all the yellow ants contained an immature stage of a tapeworm, the cestode Anomotaenia brevis. This cestode has a typical complex life cycle in which immature stages live in an intermediate host (in this case, an ant), which must be eaten by a final host (in this case, the spotted woodpecker) before the parasite can mature and reproduce in the final host, releasing eggs into the hosts feces. Plateaux then recognized that the yellow ants were, in fact, conspecifics of the larger, dark ants, and he

GASTROINTESTINAL HELMINTH COMMUNITIES OF BOBWHITE QUAIL

We found 12 species of intestinal helminths in 158 Northern Bobwhites (Colinus virginianus) in northern Florida (1983-1984). Of these, six species were common: the cestodes Raillietina cesticillus and R. colinia, the cecal nematodes Heterakis isolonche and Trichostrongylus tennis, the proventricular nematode Dispharynx nasuta, and the gizzard nematode Cyrnea colini. Four pairs of species had statistically significant numerical associations: the cestodes were negatively associated, and positive associations existed between the cecal nematodes, R. cesticillus-D. nasuta, and H. isolonche-C. colini. When either cecal nematode was present in high densities, H. isolonche shifted its location, indicating a possible negative interaction. There were some intraspecific relationships be- tween cestode density and mean location, location variance, and biomass. In addition, R. cesticillus biomass was negatively correlated with R. colinia density. This community, while not characterized by high species richness, is readily colonized and exhibits evidence of inter- and intraspecific interaction. It does not conform to current models of parasite community structure.

Evolutionary patterns of altered behavior and susceptibility in parasitized hosts

Adaptation is the usual context for interpreting parasite‐host interactions. For example, altered host behavior is often interpreted as a parasite adaptation, because in some cases it enhances parasite transmission. Resistance to parasites also has obvious adaptive value for hosts. However, it is difficult to evaluate the adaptive significance of host‐parasite interactions without considering the historical context in which these traits have evolved and if they can be predicted by host (or parasite) phylogeny. We examined the influence of host phylogeny on patterns of altered behavior and resistance to parasitism in a cockroach‐acanthocephalan system. A consensus cladogram for cockroach subfamilies was produced from the morphological data of McKittrick. We used this cladogram to predict patterns of altered host behavior in seven cockroach host species. Each species was experimentally infected with a single species of acanthocephalan, Moniliformis moniliformis, a parasite that is transmitted when cockroaches are eaten by rodent final hosts. Activity patterns, substrate choices, and responses to light were measured for control and infected animals. These data were recoded into a behavioral matrix of discrete characters. We determined the most parsimonious distribution of the behavioral characters on the tree obtained from McKittricks data. We then measured the concordance between the behavioral data and the cockroach cladogram with the consistency index (CI). We compared the observed CI to the expected value based on a randomization of observed character states. For three different models of evolutionary character change, there was no evidence of strong concordance (significantly large CI) between altered host behavior and host relationships. Parsimony analysis of the interior nodes of the phylogenetic reconstruction suggested that unaltered behavior was the ancestral state for most host behaviors. We also compared host phylogeny to a data set on the susceptibility of 29 cockroach species to infection with M. moniliformis. At the species level, there was a significant concordance between susceptibility and host phylogeny. This pattern was consistent with the finding that susceptibility of species varied significantly among different subfamilies. However, at the subfamily level, susceptibility was not strongly concordant with phylogeny. We predict that, given enough time, resistance should be lost in subfamilies that are currently resistant to parasitism. In spite of the potential importance of phylogeny in the evolution of behavior and susceptibility, we found little evidence for phylogenetic effects in this system. We conclude that changes in the behavioral responses of hosts to parasites and, to a lesser extent, changes in susceptibility are more frequent than cockroach speciation events in different cockroach lineages. This finding strengthens the assertion that at least some of the altered behaviors are adaptive for host and/or parasite.

Behavioural fever is a synergic signal amplifying the innate immune response

Behavioural fever, defined as an acute change in thermal preference driven by pathogen recognition, has been reported in a variety of invertebrates and ectothermic vertebrates. It has been suggested, but so far not confirmed, that such changes in thermal regime favour the immune response and thus promote survival. Here, we show that zebrafish display behavioural fever that acts to promote extensive and highly specific temperature-dependent changes in the brain transcriptome. The observed coupling of the immune response to fever acts at the gene–environment level to promote a robust, highly specific time-dependent anti-viral response that, under viral infection, increases survival. Fish that are not offered a choice of temperatures and that therefore cannot express behavioural fever show decreased survival under viral challenge. This phenomenon provides an underlying explanation for the varied functional responses observed during systemic fever. Given the effects of behavioural fever on survival and the fact that it exists across considerable phylogenetic space, such immunity–environment interactions are likely to be under strong positive selection.

Parasites and the behavior of biting flies

Biting fly behavior involved in parasite transmission is reviewed. Except for the areas of activity and probing, few investigations have addressed ways in which parasites might alter vector behavior. Given the manner in which parasites alter behavior in other arthropods (e.g., habitat choice, color preference), it is reasonable to expect infected hematophagous flies to behave differently from uninfected conspecifics. This could have important epidemiological consequences.

An overview of parasite-induced behavioral alterations - and some lessons from bats.

Summary An animal with a parasite is not likely to behave like a similar animal without that parasite. This is a simple enough concept, one that is now widely recognized as true, but if we move beyond that statement, the light that it casts on behavior fades quickly: the world of parasites, hosts and behavior is shadowy, and boundaries are ill-defined. For instance, at first glance, the growing list of altered behaviors tells us very little about how those alterations happen, much less how they evolved. Some cases of parasite-induced behavioral change are truly manipulative, with the parasite standing to benefit from the changed behavior. In other cases, the altered behavior has an almost curative, if not prophylactic, effect; in those cases, the host benefits. This paper will provide an overview of the conflicting (and coinciding) demands on parasite and host, using examples from a wide range of taxa and posing questions for the future. In particular, what does the larger world of animal behavior tell us about how to go about seeking insights – or at least, what not to do? By asking questions about the sensory–perceptual world of hosts, we can identify those associations that hold the greatest promise for neuroethological studies of parasite-induced behavioral alterations, and those studies can, in turn, help guide our understanding of how parasite-induced alterations evolved, and how they are maintained.

Relationships between Bobwhite Quail Social-Group Size and Intestinal Helminth Parasitism

We examined the relationships of helminth prevalence and intensity to bobwhite quail social-group size with 85 immature bobwhite quail. Although bobwhite coveys may not be cohesive in some parts of the range or during some seasons, we argue that in the sedentary populations of northern Florida, young of the year may retain covey membership until the breeding season. Among these birds, we found nonrandom associations between intensity and covey size for some parasitic helminths. This was most consistently true for the monoxenous parasite with the shortest life cycle.

Asexual reproduction in cestodes (Cyclophyllidea: Taeniidae): ecological and phylogenetic influences

Asexual reproduction, a rare trait among cestodes in general, occurs in the “larval” (metacestode) stage of species of the family Taeniidae. The distribution of this trait among taeniid species is not consistent with an ecological hypothesis of current environmental predictability. We therefore chose a subset of the family and studied their phylogenetic relationships by Wagner parsimony analysis as a test of historical influences on asexual reproduction. We produced a consensus tree based on four 50‐step trees with consistency indices of 0.38. Given these hypothetical relationships, we found that asexual reproduction either arose or was lost multiple times. Moreover, this consensus tree is incongruent with both definitive and intermediate host phylogenies, and asexual reproduction does not correlate with host transfers inferred from these phylogenies. Developmental and phylogenetic constraints on asexual reproduction therefore appear to have been minimal. Given current information, neither historical constraint nor explanations invoking adaptation based on environmental predictability can account for life‐history variation in these cestodes.