Host Manipulation by Parasites: a Multidimensional Phenomenon

Host manipulation by parasites: a multidimensional phenomenon

Frédéric Thomas, Robert Poulin and Jacques Brodeur

F. Th omas ([email protected]), Génétique et Evolution des Maladies Infectieuses, UMR CNRS/IRD 2724, 911 Ave. Agropolis, BP 64501, FR–34394 Montpellier cedex 5, France. – FT and J. Brodeur, Inst. de recherche en biologie végétale, Dépt de sciences biologiques, Univ. de Montréal 4101, rue Sherbrooke est, Montréal (Québec), H1X 2B2, Canada. – R. Poulin, Dept of Zoology, Univ. of Otago, PO Box 56, Dunedin 9054, New Zealand.

Th e diversity of ways in which parasites manipulate the phenotype of their hosts to increase their transmission has been well-documented during the past decades. Parasites clearly have the potential to alter a broad range of phenotypic traits in their hosts, extending from behaviour and colour to morphology and physiology. While the vast majority of studies have concentrated on few, often only one, host characters, there is increasing evidence that manipulative parasites alter multiple characteristics of their host’s phenotype. Th ese alterations can occur simultaneously and/or successively through time, making parasitically modifi ed organisms undoubtedly more complex than traditionally viewed. Here, we briefl y review the multidimensionality of host manipulation by parasites, discuss its possible signifi cance and evolution, and propose directions for further research. Th is view should prove to be an extremely useful approach, generating a series of testable hypotheses regarding the ecology of parasitized hosts, and leading to a better comprehension of complex host–parasite relationships.

Parasite-induced alteration of host phenotype is a wide- complex signalling systems that have fuelled recent research spread strategy of transmission among pathogens (Moore in behavioural ecology. We show how the use of conceptual 2002). It has been reported in viruses, fungi, bacteria, pro- tools borrowed from other fi elds and applied to a multidi- tozoans, nematodes, nematomorphs, trematodes, cestodes, mensional view of host manipulation can lead to progress in acanthocephalans and parasitoids (Poulin 2007, Lefèvre the study of host–parasite interactions that would otherwise et al. 2009). Phenotypic changes in parasitized hosts can vary not be possible. greatly in their magnitude and diversity, from slight shifts in the percentage of time spent performing a given activ- Defi nition of multidimensionality ity to the display of spectacular morphologies or behaviours (Th omas et al. 2002a, Yanoviak et al. 2008). While host- Basic considerations manipulative parasite associations are frequently known A fi rst condition before a manipulation can be considered for one particularly striking phenotypic change (e.g. ants as multidimensional is that at least two changes in diff er- manipulated by Dicrocoelium dendriticum climb to the top ent phenotypic traits, or in the same phenotypic traits, are of grass blades, crickets parasitized by hairworms jump observed in the manipulated host. Th ese changes can occur into water…), it is increasingly recognized that parasitically within or between trait categories (behaviour, morphology modifi ed hosts are not merely normal hosts with one or few and/or physiology), and must not correspond to diff erent altered traits, but instead they are deeply modifi ed organisms ways of measuring the same alteration. For instance, a behav- (Poulin and Th omas 1999, Brodeur and Boivin 2004, Cézilly ioural change can be associated with neurological disorders and Perrot-Minnot 2005, Th omas et al. 2005). One cause of in the brain of the parasitized host, but we cannot consider this complexity is that manipulative parasites alter not only the atypical behaviour displayed and their associated neu- one but several phenotypic traits in their hosts (Table 1). rological bases as diff erent dimensions of the manipulation. Here, we explore the multidimensional aspect of host In addition, since the label manipulation has been restricted manipulation by parasites. After providing defi nitions and to phenotypic changes that are involved in parasite trans- examples, we discuss the extent, signifi cance and evolution mission processes (Poulin 1995), we propose to also restrict of this phenomenon, and show how it provides a new and the label multidimensionality to these specifi c changes. For promising research direction. Specifi cally, we link multidi- instance, if we consider the case of the amphipod Gammarus mensional manipulation with theoretical frameworks already insensibilis parasitized by the trematode Microphallus papil- established in other fi elds, such as the mosaic theory of lorobustus (Table 1), it has been demonstrated that each coevolution, and the hypotheses regarding the evolution of of the three behavioural changes displayed by parasitized

1217 Table 1. Examples of multidimensionality in host-manipulative parasite systems (the list is not exhaustive).

Host–parasite systems Phenotypic alterations References

Crustaceans–Helminths Trematoda Gammarus insensiblis - Microphallus positive phototactism Helluy 1984 papillorobutus negative geotactism aberrant evasive behaviour higher glycogen content Ponton et al. 2005 longer intermoult duration Thomas et al. 1996 reduced fecundity and pairing success Thomas et al. 1995

Acanthocephalan Gammarus pulex - Pomphorynchus laevis presence of a new color (orange spot) Moore 2002 positive phototactism Cézilly et al. 2000 increased activity Dezfuli et al. 1994 reduced oxygen consumption Rumpus and Kennedy 1974 reduced fecundity and pairing success Bollache et al. 2002 increased glycogen levels Plaistow et al. 2001 increased heamocyanin concentration Bentley and Hurd 1996 increased level of ﬂ uctuating asymetry Alibert et al. 2002 immune depression Cornet et al. 2009

Cestode Artemia parthenogenetica - Conﬂ uaria podicipina increased lipid contents Sanchez et al. 2009a, 2009b positive photactism and unpubl. data increased carotenoid contents neurological disorders Gammarus pulex - Cyathocephalus truncates physiology and behaviour Franceschi et al. 2007 Insect–Nematomorpha Nemobius sylvestris - Paragordius tricuspidatus increased activity Thomas et al. 2002a erratic behaviour water-seeking behaviour Insect–Fungus Camponotus leonardi - Ophiocordyceps biting behaviour Andersen et al. 2009 unilateralis habitat preference

Insects–Nematodes Baetis bicaudatus - Gasteromermis sp. morphology (feminisation of males) Vance 1996 behaviour (males undergo complete sex reversal)

Cephalotes atratus – Myrmeconema sp. morphology (induce fruit mimicry) Yanoviak et al. 2008 behaviour (gasters are held in a conspicuous elevated position, reduced defensive behaviour) Insect–Parasitoid Aphidius nigripes - Macrosiphum euphorbiae negative phototaxis Brodeur and McNeil 1990 thigmokinesis selection of dark-colored substrate Fish–Cestodes Gasterosteus aculeatus - Schistocephalus solidus foraging behaviour Barber and Huntingford 1995 shoaling behaviour

Rutilus rutilus - Ligula intestinalis swim close to the surface Loot et al. 2002 aberrant response to stimulus morphology

Insect–Protozoan Aedes aegypyi - Plasmodium gallinaceum sequential manipulation: Koella et al. 2002 reduced and then increased appetite Mammal–Virus aggressiveness Rupprecht et al. 2002 Canis vulgaris - Lyssavirus hypersalivation

Mammal–Protozoan Rattus rattus - Toxoplasma gondii higher activity level Berdoy et al. 2000 hless cautious to novel stimuli attracted by the odour of cat urine

1218 individuals contribute to increase the risk of predation by host compensatory responses are diff erent but not mutually aquatic birds (defi nitive host), and hence the transmission exclusive scenarios, multidimensionality in host manipula- of the parasite (Helluy 1984). However, it remains unclear tion can also have mixed origins. whether the reduced reproductive performance of parasitized individuals and/or their longer intermoult duration also play roles in transmission. It can be advantageous for the Parasite-induced multiple manipulations parasite to shift host resource allocation from reproduction Complex alterations of host phenotype can arise from para- and growth to survival, since host survival until predation is sites being able to directly manipulate several traits in their essential for trophically-transmitted parasites (Poulin 1994, hosts. Th e manipulation of several host traits by parasites Hurd et al. 2001). In such cases, the reduced reproductive is indeed likely to be favoured by selection. For instance, performance and/or growth of parasitized hosts could be a trophically-transmitted parasite can greatly enhance the considered as a dimension of the manipulation. Otherwise, detectability and vulnerability of its intermediate host to it should be considered as a pathological consequence of the predation by defi nitive hosts if it alters simultaneously the infection. For example, while the immune depression induced behaviour and the colour of its host (Bakker et al. 1997, by the acanthocephalan parasite Pomphorynchus laevis in its Sanchez et al. 2009a). Disentangling the exact adaptive nature intermediate amphipod host Gammarus pulex improves par- of each dimension, however, is not always straightforward. asite survival within the intermediate host’s body cavity, it Consider for instance the case of crustaceans parasitized by has apparently no relation to the behavioural alterations that helminths (Table 1) for which, in addition to behavioural favour transmission to defi nitive hosts (Cornet et al. 2009). changes, an increased level of energetic reserves is observed Th e absence of correlation is however not always evidence in these host-parasite associations. Th ese parasites are phy- for the two altered traits being independent of each other. logenetically unrelated but they have evolved under similar For instance, diff erent neuro-hormones (aff ecting specifi c ecological pressures for their transmission as they require the phenotypic traits) may react diff erently to an increase in the predation of the crustacean by a vertebrate predator. If we concentration of a neuro-modulator induced by the parasite thus assume that enhanced lipid content in the crustacean in its host. host is adaptive for transmission, at least two scenarios can be proposed. First, because displaying an aberrant behaviour can be energetically costly for host species, hosts with a high Can host responses be considered to level of energy reserves could be manipulated for longer multidimensionality? periods than those with poor reserves (Ponton et al. 2005). A Poulin and Th omas (1999) argued that the ability of infected physiological manipulation of lipid metabolism could then hosts to undergo signifi cant phenotypic alterations, such as enhance the length, and thereby the chance of success, of the a change of microhabitat, may depend on the plasticity of behavioural manipulation. A second, not mutually exclu- some other traits to accommodate this novelty. Manipu- sive, explanation is possible: given that predators foraging lative parasites could then act as a developmental switch on potentially infected prey try to minimise the ratio of cost channelling several associated traits in particular direc- of infection to energetic benefi ts (Laff erty 1992), enhancing tions (Dingemanse et al. 2009). Because these phenotypic the nutritive value of the host may be selected as a parasitic adjustments are host responses, whether or not they could strategy to increase transmission to predators that are able be considered as a dimension in the manipulation is debat- to visually discriminate among prey having diff erent ener- able. Th ese changes can be benefi cial for parasitized hosts if getic values (Sanchez et al. 2009b). It appears important, they allow them to reproduce, at least partially, under their when feasible, to explore the precise nature and outcome new circumstances. Th ey can also correspond to automatic of each alteration on parasite transmission, and the way it plastic responses that are not, in the present context, associ- interacts with the other dimensions. For example, Kaldonski ated with signifi cant fi tness benefi ts for either the host or et al. (2009) tested for an eff ect of acanthocephalan parasite the parasite. Finally, they can be benefi cial for the parasite coloration (in addition to behavioural changes) on increased if they allow the parasitized hosts to cope better with new trophic transmission by painting a yellow-orange spot on environmental conditions until events related to transmis- the cuticle of uninfected gammarids and by masking the sion (e.g. predation by defi nitive hosts) occur. Th is does not yellow-orange spot of infected individuals with inconspicu- necessarily mean that the parasite induces them directly, at ous brown paint. Th ey found no evidence for a role of para- best it means that it does not suppress them. We suggest that site coloration in the increased vulnerability of gammarids to traits that are merely host responses should not be consid- predation by trout. ered as part of multidimensional manipulation, unless one can demonstrate that they are adaptively maintained by par- Simultaneous and sequential multidimensionality asites because of transmission benefi ts. Lefèvre et al. (2008) At least two types of multidimensionality must be distin- proposed that manipulative parasites could aff ect fi tness- guished: the simultaneous and the successive ones. For related traits in their hosts (e.g. fecundity, survival, growth, instance, while the phenotypic changes reported for G. competitiveness) in order to stimulate host compensatory insensibilis (Table 1) occur simultaneously, those mentioned responses, when these responses match with the parasites’ for crickets harbouring hairworms occur in succession. In transmission routes. In that case, the manipulation relies on infected crickets, the fi rst behavioural change (the erratic host responses which are triggered by the parasite. Th is type behaviour) occurs before the worm is fully mature, and of host responses should be included into multidimensional- apparently serves to increase the probability of encountering ity. Because manipulation sensu stricto and exploitation of a water body suitable for worm emergence and reproduction;

1219 about one week later, the second behavioural change enables Interestingly, diff erent evolutionary scenarios can be pro- the parasite to physically enter water (Sanchez et al. 2008). posed depending on which dimension is considered to be Th ese behavioural changes are two components of the same historically the fi rst to arise. In the previous example, it could transmission strategy but they clearly occur one after the be that positive phototaxis was the fi rst behavioural change other: crickets displaying the erratic behaviour do not yet displayed by parasitized gammarids, and the aberrant escape enter water (Sanchez et al. 2008). In a related vein, Koella behaviour only appeared subsequently. If so, we could no lon- et al. (2002) showed that diff erent stages of the malaria ger argue that positive phototaxis evolved because it reduced parasite Plasmodium gallinaceum diff erentially aff ect the the energetic costs linked to the aberrant escape behaviour. host-seeking behavior of its mosquito vector Aedes aegypti. Similarly, in the case of sequential multidimensionality, it Immature stages are expected to increase the vector’s survival is important to keep in mind that the chronology through to increase their chance of becoming mature, while mature which successive dimensions are actually observed may, or stages are potentially confronted with a tradeoff between may not, refl ect the order in which they appeared during the increasing the vector’s lifespan and thus survival on the one course of evolution. For this chronology to be the same as the hand, and on the other increasing biting frequency at the observed order, it is necessary that each dimension has in itself expense of survival since biting is risky in nature. Accord- a positive eff ect on transmission. Conversely, when the chro- ingly, mosquitoes parasitized with oocysts (which cannot be nology is not the same, the hypothesis that certain dimen- transmitted) are less likely to seek further probing, conversely sions evolved as secondary adjustments becomes a possible to individuals infected with transmissible sporozoites. scenario. In this case, the fi rst dimensions currently observed do not necessarily have a direct value for transmission. Multidimensional manipulations: evolving from Another way to improve the effi ciency of a given manipu- unidimensional ones? lation is to reduce the probability of the intermediate host being eaten by unsuitable species. Th ere are several studies From an historical or phylogenetic perspective, manipula- illustrating that certain features of parasite-induced behav- tive parasites derive most likely from non-manipulative ones, ioural changes seem more targeted at limiting the risk of pre- and it is more parsimonious to assume that the original dation by the wrong (non-host) predators than at increasing manipulation involved only one dimension. Any individual transmission to appropriate hosts (Levri 1998). For instance, parasite able to modify one dimension of its host phenotype the acanthocephalan Polymorphus minutus, which completes with a resulting increase in its transmission success would its life cycle in aquatic birds, does not only alter the behav- have been favoured over its conspecifi cs by natural selection. iour of gammarids in a way that increases their probability Given enough genetic variation, what originally may have of being eaten by birds, it also enhances the escape perfor- been an incidental side-eff ect of infection could then have mance (swimming speed increases of up to 35%) of parasit- been shaped by selection into a refi ned manipulation mecha- ized individuals when facing non-host predators, especially nism (Poulin 1994). Disentangling the mix of adaptive forces the crustacean predator Dikerogammarus villosus (Medoc that shaped the transition from a simple manipulation to a and Beisel 2008). Several studies have failed to fi nd adap- multidimensional one off ers a great challenge. Th ere are tive responses of trophically transmitted parasites against indeed several selective forces that can explain why fi tness non-host predators (Mouritsen and Poulin 2003, Kaldonski benefi ts are gained by adding dimensions to a simple manip- et al. 2008). However, recent empirical and theoretical studies ulation. show that the avoidance of non-hosts is not always favoured Th e addition of a novel dimension to a simple manipula- by selection because despite the costs incurred, host manipu- tion is likely to be favoured when the transmission benefi ts lation may still be advantageous for the parasite (Seppälä and compensate for the extra costs of any new dimension. Th is Jokela 2008, Seppälä et al. 2008, Parker et al. 2009). situation is particularly likely when the interaction between Within an evolutionary perspective, the capacity to manip- the two dimensions boosts the transmission in a synergis- ulate several host traits could be inherited from an ancestor tic fashion. Selection likely favours the addition of novel of the parasite (Moore and Gotelli 1990). For this reason, the dimensions when it improves the effi ciency of the original evolution of mutidimensionality must be envisaged within a one. For instance, in the case of G. insensibilis (Table 1), the phylogenetic context, just like simple manipulations (Poulin aberrant escape behaviour displayed by parasitized individu- 1995). In cases where multidimensional manipulations did als consists in swimming at the air/water interface each time not evolve independently (i.e. they are ancestral legacies), there is a mechanical disturbance in the water (like a foraging their adaptive value can however be maintained since they bird walking). Such a behavioural change, on its own, would still increase signifi cantly the probability of successful trans- be likely to increase mortality in parasitized gammarids as mission. When similar traits are induced by phylogenetically mechanical disturbances are not always caused by birds and unrelated parasites experiencing comparable selective pres- multiple displacements between the bottom and the surface sures (see for instance Crustaceans and manipulative helm- would result in a waste of energetic reserves. Th is non-adap- inths, Table 1), convergence is a reasonable explanation since tive outcome can be avoided if parasitized gammarids also a similar manipulation of host behavior could have arisen display a positive phototaxis causing them to stay at the water independently in diff erent parasite lineages. surface. Although further experimental evidence would be necessary to support this statement, it seems plausible that Multidimensionality from a mechanistic perspective once a dimension has been retained by selection, then selection is likely to favour adjustments (i.e. other dimensions) One way to explore how diff erent dimensions could be mech- that improve its effi ciency by reducing the associated costs. anistically related would be to study correlations between

1220 the extent of modifi cation in diff erent altered traits. Such an transmission processes. A second promising research direc- approach has rarely been adopted until very recently. Benesh tion would be to determine the precise function of each trait et al. (2008) studied fi ve traits from individual isopods in multidimensional manipulations, as well as the way their infected by the acanthocephalan Acanthocephalus lucii (hid- interaction (additive or synergistic) boosts transmission suc- ing, activity level, substrate colour preference, anterior and cess. Th is would then also allow us to evaluate the relevance posterior body colorations). Infected isopods hid less and of the hypothesis according to which certain dimensions had darker abdominal coloration than uninfected isopods. evolved not because they increase transmission, but because However, these two modifi ed traits were not correlated, they reduce the cost of previous dimensions. which suggests they may have arisen via independent mecha- A full understanding of the evolution of the multidimen- nisms. Similarly, in laboratory experiments Helluy (1984) sionality of manipulation also requires knowledge of the showed that in G. insensibilis parasitized by M. papillorobustus selective pressures experienced by both the host and the par- (Table 1), negative geotaxis, positive phototaxis and aberrant asite. We thus encourage researchers to consider the ecologi- escape behaviour can all occur separately. cal context in which multidimensional manipulations occur At the moment, it is unknown for the vast majority of (Th omas et al. 2005). Th is is critical to our understanding multidimensional manipulations whether multiple changes of the costs and the benefi ts of parasitic manipulation. In in host phenotype are mechanistically related or indepen- some cases, certain features of parasite-induced behavioural dent. Positive correlations could indicate that parasites aff ect changes seem more relevant to limiting the risk of preda- one particular component of the host’s physiology which tion by the wrong (non-host) predator than to increasing results in a cascade of eff ects. In such a case, all alterations transmission to appropriate hosts (Levri 1998). Th ere are might not be equally effi cient in enhancing transmission to other ways in which environmental forces can drive mul- appropriate fi nal hosts, some of them eventually making tidimensional manipulation. For example, on a geographi- parasitized intermediate hosts more vulnerable to preda- cal scale, populations of the same parasite species infecting tors that are inappropriate fi nal hosts (Cézilly and Perrot- diff erent host populations will experience diff erent selective Minnot 2005). For this reason, it appears important, when forces, because of regional variation in community composi- possible, to explore the independent eff ects of each alteration. In some areas, one species of defi nitive host may be the tion on parasite fi tness. Manipulative parasites can also alter dominant predator of intermediate hosts; in another area, several physiological pathways independently. Unless para- another suitable defi nitive host species may be numerically sites are limited in their ability to alter more than a single dominant, and in yet another locality suitable defi nitive dimension in their intermediate hosts, no signifi cant correla- hosts may be outnumbered by non-host predators. Simi- tion in magnitude are expected between traits (Cézilly and larly, the variety of microhabitats available to manipulated Perrot-Minnot 2005). Th e majority of studies assume that intermediate hosts may vary greatly among localities, such costs are inevitably associated with manipulation. Although that one altered trait that works effi ciently for the parasite this assumption is reasonable, at this stage, speculation has in one area may be ineff ective or costly (in terms of inges- proven more attractive than data collection. Th is gap cur- tion by non-hosts) elsewhere. Parasites coevolve with their rently limits our understanding of the evolution of manipu- hosts in a heterogeneous environment, following the general lative processes (uni- or multidimensional ones) based on principles of the geographic mosaic theory of coevolution this assumption. (Th ompson 2005). Th erefore, multidimensional manipulation may have evolved, and may be maintained, in response Conclusion and future directions to spatially variable external conditions aff ecting the probability of transmission. Th e panoply of traits manipulated Compared to the important eff ort invested in the study of by a parasite may increase the probability that at least one of host manipulation by parasites, relatively few studies have these manipulated traits will fi t the current local conditions. explored its multidimensional character. At the moment, Measuring the benefi ts of diff erent altered traits under dif- this phenomenon is mainly known from a descriptive point ferent external conditions would provide a promising way to of view, and probably also only refers to biological models assess the adaptiveness of multidimensionality. for which its detection was easy. An immediate challenge Hosts in nature are usually infected by multiple phylo- will be then to gather more systematic information on the genetically unrelated parasites, which may have opposing range of host-manipulative parasite systems in which multi- interests in their use of the host. In certain cases, parasites dimensional manipulation is manifested, and on the range of have been shown to sabotage the manipulation exerted by traits that are altered in each case. Because multidimensional other parasites, reverting the phenotype of an infected hosts manipulations are diversifi ed and complex phenomena, to its ‘normal’ uninfected state (Th omas et al. 2002b, Haine one single method or model cannot totally describe them. et al. 2005, Rigaud and Haine 2005). It would be interesting Researchers interested in multidimensional manipulation in these situations to explore whether or not sabotages apply must engage in greater exchanges and collaborations with to all the dimensions of a multidimensional manipulation, colleagues who understand how physiology, neuroanatomy or only those that are the most critical for the transmission and ‘omics’ contribute to phenotypic trait expression. Th is interests of the sabotaging parasite. step is essential before generalisations can be made. Th en, From a mechanistic perspective, nothing is known con- a fi rst exciting research direction would be to explore, via cerning the way multidimensional manipulation occurs. comparative studies, whether the nature of altered trait com- Th is research direction therefore has huge potential, and binations is linked to the phylogenetic affi nities of hosts, could benefi t from sophisticated approaches such as the of parasites and/or to the ecological constraints linked to incorporation of post-genomic tools for determining the

1221 genetic basis of manipulation. Th is will help to predict if Bakker, T. C. M. et al. 1997. Parasite induced changes in behaviour host traits modifi ed by manipulative parasites should covary and colour make Gammarus pulex more prone to fi sh preda- positively or negatively in magnitude. An interesting avenue tion. – Ecology 78: 1098–1104. will also be to explore the possible mechanistic links between Barber, I. and Huntingford, F. A. 1995. Th e eff ect of Schistocephalus solidus (Cestoda: Pseudophyllidea) on the foraging and shoal- the multidimensionality of host manipulation and the host ing behaviour of three-spined sticklebacks, Gasterosteus aculea- immune system. tus. – Behaviour 132: 1223–1240. Host manipulation as a scientifi c fi eld has, until now, Benesh, D. P. et al. 2008. Multidimensionality and intra-individual developed in relative isolation from behavioural ecology variation in host manipulation by an acanthocephalan. – Para- approaches. Th is is unfortunate since links between these sitology 135: 617–626. fi elds have the potential to reveal new perspectives and lines Bentley, C. R. and Hurd, H. 1996. Carbohydrate titres in the hae- of research. Complex signal function has indeed been stud- molymph and midgut glands of Gammarus pulex infected with ied in many species by behavioural ecologists, and therefore, the acanthocephalan Pomphorhynchus laevis. – J. Helminthol. 70: 103–107. examples of animals in which signallers use more than one Berdoy, M. et al. 2000. Fatal attraction in rats infected with Toxo- display to advertise their qualities are common (Møller and plasma gondii. – Proc. R. Soc. Lond. B 267: 1591–1594. Pomiankowski 1993). Th ree hypotheses are usually invoked Bollache, L. et al. 2002. Eff ects of two acanthocephalan parasites to explain why these complex signals evolve. 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