Host manipulation by parasitesDavid P.Hughes, JacquesBrodeur, and FrédéricThomas, eds Oxford University Press, UK

The book is a beautiful combination of expert thinking and knowledge on parasites exploiting multicellular host individuals, populations, societies and communities, as their ecosystem. The book comprises eleven chapters by expert behavioural ecologists as main authors, each one appended by an afterword from a nonbehavioural ecologist, a briefer reflection on the main authors' treatment. Reading this book can entertain any biologist's curiosity for the ubiquitous phenomenon of parasitism, and especially animal behaviour manipulation by microbial or animal parasites. I would recommend it or at least parts of it as reading to undergraduates taking introductory zoology, or as a main source for graduates in ecology, evolutionary biology, animal parasitology, medical and veterinary sciences, and biodiversity conservation. In the book foreword, Dawkins reminds us of his extended phenotype paradigm, which sets the host organism from the evolutionary viewpoint of the parasite: the parasitized host phenotype is ‘bended to a direction hostile to the host's own genes’. But hostility varies widely across parasitic phenomena from negligible or benign, to stressful but tolerable (reduced growth and reproduction), and in extreme cases to host suppression either reproductively or completely (death) thus freeing the parasite into a dispersal stage. Parasitism is most intricate for multi-host parasites with complex cycles whose final (reproductively) host is a predator. The life style of Dawkins' Verticobacter seems to match that of Toxoplasma gondii in its parasitic relation to humans (see Chap 10, and below). As opposed to its lifestyle in primary host rodents, Toxoplasma in humans seems not to trouble with sex, its persistence being delegated to our viviparous reproduction ensuring direct continuity between mother and infant as successive hosts in the parasite's life. In Chapter 1, Moore tells us an informative story of how and when traditional parasitology recently became ‘cool’ or popular. Parasites at a node point of their cycle and making their host especially appealing to a predator were thought of as manipulators well before the ‘cool age’ (Moore cites Siebold 1853 on mode of transfer of Leuchochloridium to its next host). Like for other organisms, there is no goal or direction in parasite evolution. Thus, there is no support for benign parasites consistently emerging from brutal ancestors. A pattern with more support is that relatively small parasites, which reproduce in the host, are selected more rapidly and evolve more often to sympatric speciation. Compilations by Moore indicate that parasites and their altered hosts became popular in the late 1900's, following the birth of many ecology journals. Moore reviews altered host behaviours that do not benefit parasites, such as vertebrate avoidance/defence against biting flies, self-medication and grooming, anorexia, sleep and ‘depression’ redirecting host resources to combat pathogens and ectotherms’ behavioural fever with similar effects. Moore says we must thank behavioural ecologists for revealing the ‘cool side’ of parasites that make their hosts behave strangely. Part of Moore's exposé tells us of the many scientist women who have been leaders in parasitology, including ‘cool’ aspects such as induced host suicide as a key event in parasite transmission to predators, and the role of parasitism in sexual conflict (mate choice). Afterword author Alcock also praises the contribution of behavioural ecology to parasitology, pointing out the very productive and influential idea that female mate choice (in e.g. birds), may have evolved because of variable susceptibility to parasites among males. In reviewing evolutionary routes to manipulation in Chapter 2, Thomas, Rigaud and Brodeur consider two scenarios of parasitized host behaviour evolution, that is, parasite-driven (most studies) and host-driven, for example compensatory foraging or mating. As parasites first evolved from free-living ancestors, the second scenario seems more likely. Ancestral parasites were probably surviving and exploiting abundant resources in the digestive, aerial, or coelomic body cavities of accidental hosts. As pointed out, enhanced naturally iterative host behaviours such as sex and foraging can benefit fitness of both host and parasite, as demand-driven compensating behaviours. When even brief parasitism allows parasite survival and growth or reproduction, traits favouring parasitism durability and fixation, including host manipulative traits, are strongly selected. Interactive manipulation should persist as a ‘cool’ topic in parasitology, as parasitized hosts are relatively easy to observe, although they are in fact complex evolving units with intraspecific variability arising at multiple levels between genomes, species stages, sexes and morphs of the hosts and parasites. Afterword author Stearns expectedly addresses manipulation within the context of life cycle evolution. A panoply of evolutionary ideas can emerge when our thinking switches from individual organisms to interactions involving not only the individual with the other sex, family or group members, stages and morphs within a species, but also with heterospecific symbionts, mutualists, pathobionts and parasites. The close associations they form with the host involve each one's phenotype (and genotype) and range more or less widely on the symbiosis spectrum. Each one constitutes a regular and reliable external feature of the other's environment, which determines their fitness. Stearns suggests that host manipulation by a parasite evolves when a previously dispersive stage establishes in a potential next host, to which it then ‘delegates some of its fitness traits’. Coevolution eventually eliminates traces of the original dynamics, leaving us with an egg-chicken puzzle. In Chapter 3, Adamo reaches into the fine strings of behavioural manipulation, with examples from the famous or infamous ‘puppet masters’, such as brain cysts-forming Toxoplasma manipulating rodents into being easier prey for their cat enemies. Even with good reasons for behavioural alterations having a parasitic or symbiotic cause, we should never be content until a clear biological mechanism has been identified and properly tested. If a nematomorph worm indeed has the tools to drive the oriented move of a cricket towards a body of water and then to take a bath so that the worm finally reaches its aquatic reproductive milieu, then the mechanical linkages between the worm driver and the cricket vehicle must be described and shown to explain the original detour (Ponton et al. 2011). The ‘explanation’ of the fitness advantage for the worm is not satisfactory, convincing and conclusive. We are still left with mostly indirect and obscure mechanisms at work between the two animals. One might suggest for instance that host ‘hygienic bathing’ possibly explains the facts more parsimoniously than parasite manipulation. The cricket, which may survive, rids itself of its wormy ‘master’ while entering the water. Adamo exposes that infection-related immune modulation (via e.g. cytokines) alters vertebrate neural function in multiple and complex ways, inducing sickness, fatigue and irritability, a system that parasites could evidently exploit, if not manipulate. The author briefly summarizes (Table 3.2, p.45) known effects of parasites in terms of neural anatomy, chemicals and immune factors, giving us a rather unconvincing picture of how parasites could do it. Parasites do not seem to target specific neural sites and even brain cysts lodge in places that are not involved in complex behaviour. Parasites may rely on analogue chemicals of their own, acting on host behaviour status or mode with biogenic amines (dopamine, serotonin), thus acting on host neuromodulator pathways, but this still seems far from effectors of sensory-driven oriented locomotion. Afterword author Robinson reminds us that behaviours are either instinctive or experiential. If host neural effectors predictably change with infection or parasitism, then we could learn about behaviour manipulation by noxious symbionts from the induced changes. Appropriate behaviours occur as responses to stimuli at the right time and place. If behaviours evolved to be rewarding, then Robinson asks how do parasites cause host suicide? One might suggest that cell apoptosis in multicellular organisms could help us understand. Apoptosis occurs as a genetically built-in defence in immune reactions or when cells become ineluctably damaged by disease or noxious agents (Norbury and Hickson 2001). At the supra organismic level, individual worker suicide could possibly evolve to the same ultimate colony ‘curing’ effect as cellular apoptosis, as an evolutionary response to consistent and reliable experiences of attack by noxious invaders. In Chapter 4 on the behavioural ecology of parasitized hosts, Roitberg uses the power and freedom (beyond that of experimental work) of modelling to look into the question of host manipulation from a holistic perspective. Focus is on foraging decisions of hosts experiencing internal (e.g. energy level, growth) and environmental (stochastic) constraints, with or without parasitism and manipulative behaviour. Stochastic, dynamic state variable models can address host manipulation in all its useful complexity, the host role being taken here for convenience by a caterpillar using its natural foraging repertoire. The interplay of environmental heterogeneity and state dependency of both host and parasite is examined in a behavioural ecology context. The caterpillar can alter its use of nutrients and its feeding, foraging and dispersal rates either under its own control or the parasite control. Afterword author Dubois praises the focus on variation between host individuals, that is, the basis of evolutionary change, in examining fitness costs and benefits, to determine whether host behaviour alteration benefits host or parasite. On commonly depressed parasitized host feeding, Dubois comments that because immunity and growth can be traded off in a host, variation on the optimal behavioural landscape can help us answer the key question, that is, who is causing host behaviour alteration? In chapter 5 on plants manipulation, Mescher focuses on the hospitality (or inhospitality) of higher plants to parasites such as aphids, caterpillars and fungi, as manipulators. Plants are evolutionarily experienced multicellular hosts to many organisms, especially insects. The ‘green lineage’ as a eukaryotic main branch evolved as autotrophs via hospitality to photosynthetic cyanobacteria, residing today as permanent organites in all plant cells, such as the chloroplasts. Mesher points out that long-lived vascular plants, especially trees, literally define natural habitats, supporting millions of microbial and small multicellular consumers and residents. Plant individuals or clones as hosts to communities of smaller organisms are exceptionally reliable, both spatially and temporally. In contrast to most multicellular animals, plants do not move and their ‘behaviours’ generally occur at rates orders of magnitude slower than animals. Focus is on plant phenotypes that specifically improve plant quality for insects, for example, growth pattern, providing shelters such as galls, fuel for flight as nectar or take-home fast food as pollen, and that are shaped by selection on herbivore genes. These plant traits are the insect's extended phenotype sensu Dawkins, that is, they are plant traits adaptive to the insects they house (Danks 2002). Herbivore insects as plant parasites can thus become ecosystem engineers (Jones et al. 1997), with effects extending to the community level (Agrawal et al. 2012). Plant galls and insects inducing them have long been notorious as a case of heterospecific manipulation. Galls as plant structures produced ‘for the good of another species’ is an observation Darwin wrote he could not explain by Natural Selection. Galler insects can even induce extra floral nectaries, thus recruiting ants as bodyguards. Phylogenies show that related insect gallers induce similar galls on different plants, and gallers produce specific galls on the same plant. Gall induction is known to be under control of galler genes, which remains to be seen in host behaviour manipulation by parasites. Mesher reviews other fascinating aspects of plant manipulation by parasites. An interesting aspect having little appeal for ecologists interested in overt behaviour is plant defence signalling governed by phytohormones (salicylic acid, jasmonates, ethylene). Antagonisms, chemical trickery and cross talk are key interactions in the quiet and silent life of manipulators such as and such as and life in plants to evolving original sexual reproduction and for example, by manipulating small and especially insects with a for or sex et al. as with in traits being by plant parasites. plant (e.g. to which use for afterword author plant manipulation has evolved to as manipulators (see reliable interactions on relatively plants and their multiple insect are the of evolutionary is overt in animal hosts, but in host plants, its manipulation has more and effects. Plants commonly house multiple from We to and interactions that the higher plants a stage In Chapter and focus on manipulative in parasites, costs to hosts often with host The is examined from parasite to and to by the is on traits of parasitic exploiting host and and parasites. has been known for a long time in and has evolved at least providing support for its to parasites. with and modelling have The most hosts are by that are the most with to host and and experimental (Table of parasite to host as evolutionary on for and are on adaptive variation of host and the that parasitic learn to host trickery other than has also been may be by to chemical in insect parasites or by exploiting natural in host such as for of host is less either because of host against parasitic of is or has not been But occurs in on and and must feeding, a different than often than host are a group of host specific parasites whose match their host with host might to of that is, and more or parasites can to different hosts on to host and by or The to between of and and evolutionary of host manipulation by would not to of Afterword author by evolutionary about how natural in the context of may have to such as or insects, or parasites, would a less case of rather than recently to the for in into the but the suggest that host known as in parasites, have evolved rapidly and probably form associations to that and in the context of for if not for evolution, be to the of in in parasitism could do more than the traditional of that is, mechanisms and In Chapter and microbial symbionts on as manipulators of hosts, but also briefly insect and of is an of insects, and in to and is known to host reproduction, especially behaviour its transmission across host (see phenotypes of hosts are of especially with female and causing sex and hosts are as generally as via female and manipulators host defence and host mate choice on and host reproductive fitness towards or to hosts. These effects often have direct evolutionary via reproductive to speciation. has been in hosts including and Afterword author says he involved in the of the species complex of as a of the symbionts in this species and the role of as and In reproduction mechanisms at work in this it is still to in the In Chapter focuses on manipulation of insect as whose phenotype from of individuals reproductive and such as in and and to as to but the idea has with In the level of selection individuals and their the of the group and to not in or for example, and among by the the that parasites in by making colony as of parasite genes. But natural selection not on the as a insect colony can its worker in response to parasitism, a form of at the not all behavioural induced by parasites are (e.g. that are adaptive examples of how the (or of an individual host can be by parasites. In ants for example, parasitized may to of thus the of leaving the many parasites to out to a parasite or make it to a next host, a predator of the many the most parasites of insects are entering and among insect These parasites flies, and revealing the and evolutionary that and insect parasites have no permanent host and are not parasites sensu but in as and consumers of the the food resources (e.g. or as microbial symbionts in levels of host in and behaviour on close signalling and with or as that of the parasites of a to address the and effects of parasites and at which the of colony into into the of colony In the the to a range of from to such that the level at which traits emerge must be ants should not be they have or no parasites, in contrast with for example and the which house communities of parasites. of have mechanisms such as chemical or behavioural which parasites have to to be and especially to worker behaviour. In Chapter and for behavioural manipulation to have and evolutionary on the of parasites and the of their hosts. Like in the they the between to the parasite to the behaviours the host and having community effects are well for example on on to control have on modelling the of such effects and examining of parasitism in host taking host parasitic and can host and susceptibility to on the between hosts and the most and popular a nematomorph are more to prey to in the move the energy on by the cricket to aquatic cysts in and using as final host can and the on A similar story is for parasites of which are on to to and between and ecologists can the to of and using small as final hosts and their the level of to afterword author to state how our knowledge of the of parasites still points out that in and that for parasites must be than for their hosts. they may control hosts via thus and We must change our of parasitized hosts, and not change from them as to them as for parasite genes. We must them as in which they only a is consistent with in and microbial The being to is to ecosystem manipulation is and evolutionary change in the small has the to become a within it. In Chapter 10, and potential on and and animal and with a picture of how manipulators can the of by an the behaviour and in infection by host and making easy prey to how animal and behavioural ecologists would a same with different of parasites by or other insects, for example, are cases of behaviour of the insect their hosts can transmission at to different in such cycles is an interesting case of vertebrate behaviour manipulation by an parasite. Toxoplasma of humans behavioural effects in hosts support their specific role in the of transmission to the natural final hosts. humans also behavioural and being final hosts for sexual reproduction of the parasite. and including have to medical and in the of The that to mechanisms involved in we must focus on traits that have been selected for in the natural hosts. In the afterword and contrast and behavioural in their of hosts behavioural attack must that is, the or it. If vertebrate behaviour has been the target of manipulative parasites, then we neural at the basis of behaviour to under If evolved host traits related to and and are the natural then how behaviour without manipulators is and to the for in that to a immunity to be by disease If is so today even in societies as a and more or less benign we have not the evolutionary against it as a parasite. A answer to this towards the parasite being on the evolutionarily to symbiosis with gondii as a is in with facts about its in that is, it can be at levels of brain it is that is, humans are hosts for sexual reproduction, but it to their as a disease et al. and so it is to persist in In the and consider behavioural manipulation its that is, manipulation by parasites. behaviours as a to In evolutionary they manipulation in free-living organisms by from example using to to manipulation, that is, as direct control of behaviour at the source in the manipulation, reasons it can be as in terms of benefits to manipulators. should be the focus on parasite most animal interactions involve manipulation, especially and parasitism and close explains of its role in behavioural (and manipulation. fitness in parasitism, is against hosts. and benefits in interactions between free-living organisms example are not generally and as in parasitism and especially for which the is the evolutionary aspects of manipulation in free-living species that make them to of costs and benefits, variability in and and role between In the says that by is that can cause a to in the On the response is the range of natural the question if manipulative behaviour in free-living species is similar to parasite manipulation, towards the no its own for internal parasites. have direct signalling to the of host in contrast for example, parasites manipulating host for which it is the host overt behaviours as such that must be of eukaryotic on evolved from the of that became permanent within In parasitism in microbial a and phenotype is from the of the of a parasite (or a with that of its As the basis of its the parasitized host first has its own and then that of the parasite. the host as the extended phenotype of the parasite (or the is interesting as a thought but has as parasitized host behaviour be in its Natural selection has on the of both the parasite and the host to control behaviour in the parasitized host the from to phenotypes on each of a such as on in this book should help us the basis of host manipulation to its fitness in the of parasites. I thank for useful comments and on an of this

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