Host Manipulation by Parasites: Cases, Patterns, and Remaining Doubts

Abstract

Parasites must overcome host immunity and change hosts for dispersal. Therefore, seemingly odd behaviors of parasitized animals, like those exhibited by "Zombie ants" or the "fatal attraction" of mammals to their predators, have been explained as the extended phenotype of parasites that manipulate their hosts for transmission enhancement. Manipulation has evolved in all major phylogenetic lineages of parasites but is not ubiquitous. In fact, the real frequency and relevance of manipulation is still matter of debate. Here, I highlight some of the most pertinent questions that arise if we aim at a broader understanding of the ecological relevance and evolutionary trajectory of manipulating parasites. Why are more parasites with a trophic mode of transmission manipulating their host than horizontally transmitted parasites? Why are the causal agents of sexually transmitted diseases (STDs) so rarely reported to manipulate their host? Why do parasites of animals usually manipulate their intermediate host, whereas many pathogens of plants manipulate their final host and then cause a "fatal attraction" of herbivores to the already infected plant? How can we distinguish manipulation effects from adaptive host responses to parasitization? Does manipulation cause a cost to certain parasites that can select against the evolution of manipulation? More emphasis should be put on direct comparisons among parasites of animals, plants, and humans. Manipulation for transmission enhancement should be studied in concert with manipulation for host immunity suppression, the molecular mechanisms that control the manipulation effect need to be deciphered, and we should test for alternative explanations for the observed phenotypic changes. Finally, we should quantify transmission rates and net fitness for manipulating and non-manipulating parasites, in ecologically realistic setups, to identify the forces that select against the evolution of manipulation. Ultimately, parasite net fitness represents the relevant outcome of any manipulation effect.Keywords: immunity, malaria, partner manipulation, pathogen, plant-enemy interaction, STDs, toxoplasmosis "FATAL ATTRACTION" AND MANIPULATING PARASITES Parasites represent a ubiquitous aspect in the life of multicellular organisms (Wood and Johnson, 2015) and most, if not all, of us have experienced how strongly an infection can interfere with our normal activities and well-being. Therefore, it might not appear to be too surprising when parasitized hosts exhibit behavioral alterations (see Glossary) as compared to healthy conspecifics.

Adaptive parasitic manipulation as exemplified by acanthocephalans

“…One of the most remarkable results of species interactions in the animal kingdom is the changed appearance, behaviour or reproduction of individuals infected with parasites (Heil, ; see supplementary Table S1 for parasite‐induced trait changes by Acanthocephala). Such alterations are often induced by parasites with a complex life cycle that infect intermediate hosts (Heil, ; Moore, ; Poulin & Maure, ). Here, parasite transmission requires that the intermediate host is eaten by a further intermediate host or the final host, leading to the death of the intermediate host.…”

“…There exists considerable scepticism as to the evidence for parasitic manipulation (see, e.g., Heil, for discussion). Criticism includes: (i) the abnormal (altered) phenotype of the intermediate host is not the consequence of infection but the cause (abnormal phenotypes become easier infected); (ii) intermediate host phenotypic alterations are not adaptive for the parasite and should be considered as pathological effects, which are not adaptive to either host or parasite.…”

“…Classifying the manipulation as adaptive requires knowledge of the benefits and costs to the parasite and the host. As Heil () stated “Ultimately, parasite net fitness represents the relevant outcome of any manipulation effect.” The crucial measure for a successful manipulation is thus the increased transmission rate of the parasite due to the manipulation. Table S1 summarises the evidence of such manipulation‐based increase in transmission rate.…”

“…Usually, only the direct effects are considered manipulation. In a recent review, Heil () summarised that “Only the demonstration that a certain phenotypic alteration in the host is under the genetic control of the parasite and that it enhances the fitness of the parasite via an enhancement of its transmission rate, while decreasing the fitness of the host, would provide clear evidence in favour of adaptive host manipulation.” According to this definition, indirect effects of parasites may also be called manipulation as long as they are under the genetic control of the parasite. The distinction between direct and indirect effects and who is responsible for the effects has proven to be difficult (Thomas et al., ).…”

Behave in your parasite’s interest

“…Definitions of direct parasitic manipulation, therefore, also demand that the adaptive alteration of a host phenotype is controlled by the parasite's genotype. Parasitic manipulation must therefore be seen as an extended phenotype of the parasite (Heil 2016). Doubts about direct manipulation by parasites has particularly been raised in parasite systems in which the parasite extracts high amounts of energy from its intermediate host,…”