Fear of natural enemies in non-human animals is a concept dating back to the time of Darwin. Now recognized as a nonconsumptive effect, the ecological and evolutionary impact of fear has been studied in a number of predator-prey systems within the last few decades. However, comparatively little consideration has been given to the nonconsumptive effects that parasites have on their hosts, which have evolved behaviors to avoid parasites, impacting habitat selection, mate choice, and foraging activity. These avoidance behaviors create a “landscape of disgust”, wherein hosts navigate to avoid parasites, akin to the “landscape of fear” in prey. Evolutionarily speaking, however, predators and parasites are but two examples of natural enemies. Pathogens, parasites, predators, and parasitoids, among others, each exert their own fitness cost on the victims they attack. Since animals likely evolve in the presence of multiple natural enemies, they must adopt a range of avoidance behaviors to navigate through the resulting “landscape of peril”. Therefore, in line with recent efforts to combine the landscapes of fear and disgust, we offer a theoretical framework to better understand the impacts of natural enemies on the evolution of trait-mediated avoidance behaviors in animals. More precisely, we look at how victims may evolve to allocate energy optimally among distinct avoidance behaviors under the selective pressures imposed by different types of natural enemy. This framework is then put into the more realistic context of a food web, which highlights the impact of trophic interactions and trophic level on the evolution of avoidance behaviors.

Mermithids (phylum Nematoda) and hairworms (phylum Nematomorpha) somehow drive their arthropod hosts into water, which is essential for the worms' survival after egression. The mechanisms behind this behavioural change have been investigated in hairworms, but not in mermithids. Establishing a similar mechanistic basis for host behavioural change between these two distantly related parasitic groups would provide strong convergent evidence for adaptive manipulation and insight into how these parasites modify and/or create behaviour. Here, we search for this convergence, and also contrast changes in physiology between hosts infected with immature and mature mermithids to provide the first ontogenetic evidence for adaptive manipulation by disentangling host response and pathology from the parasite's apparent manipulative effects. We used SWATH-mass spectrometry on brains ofForficula auricularia(earwig) andBellorchestia quoyana(sandhopper), infected with the mermithidsMermis nigrescensandThaumamermis zealandica, respectively, at both immature and mature stages of infection, to quantify proteomic changes resulting from mermithid infection. Across both hosts (and hairworm-infected hosts, from earlier studies), the general function of dysregulated proteins was conserved. Proteins involved in energy generation/mobilization were dysregulated, corroborating reports of erratic/hyperactive behaviour in infected hosts. Dysregulated proteins involved in axon/dendrite and synapse modulation were also common to all hosts, suggesting neuronal manipulation is involved in inducing positive hydrotaxis. Furthermore, downregulation of CamKII and associated proteins suggest manipulation of memory also contributes to the behavioural shift.

In an era where some find fake news around every corner, the use of sensationalism has inevitably found its way into the scientific literature. This is especially the case for host manipulation by parasites, a phenomenon in which a parasite causes remarkable change in the appearance or behaviour of its host. This concept, which has deservedly garnered popular interest throughout the world in recent years, is nearly 50 years old. In the past two decades, the use of scientific metaphors, including anthropomorphisms and science fiction, to describe host manipulation has become more and more prevalent. It is possible that the repeated use of such catchy, yet misleading words in both the popular media and the scientific literature could unintentionally hamper our understanding of the complexity and extent of host manipulation, ultimately shaping its narrative in part or in full. In this commentary, the impacts of exaggerating host manipulation are brought to light by examining trends in the use of embellishing words. By looking at key examples of exaggerated claims from widely reported host–parasite systems found in the recent scientific literature, it would appear that some of the fiction surrounding host manipulation has since become fact.

Certain species of parasites have the apparent ability to alter the behaviour of their host in order to facilitate the completion of their own life cycle. While documented in hairworms (phylum Nematomorpha), the ability for mermithid parasites (from the sister phylum Nematoda) to force hosts to enter water remains more enigmatic. Here, we present the first experimental evidence in a laboratory setting that an insect which normally never enters open water (the European earwig Forficula auricularia) will readily enter the water when infected with a mermithid nematode (Mermis nigrescens). Only adult mermithids appear capable of inducing this polarising shift in behaviour, with mermithid length being a very strong predictor of whether their host enters water. However, mermithid length was only weakly associated with how long it took an earwig to enter water following the beginning of a trial. Considering the evidence presented here and its alignment with a proteomic investigation on the same host–parasite system, this study provides strong evidence for adaptive behavioural manipulation and a foundational system for further behavioural and mechanistic exploration.

Environmental stability can have profound impacts on life history trait evolution in organisms, especially with respect to development and reproduction. In theory, free-living species, when subjected to relatively stable and predictable conditions over many generations, should evolve narrow niche breadths and become more specialized. In parasitic organisms, this level of specialization is reflected by their host specificity. Here, we tested how host specificity impacts the reproductive strategies of parasites, a subject seldomly addressed for this group. Through an extensive review of the literature, we collated a worldwide dataset to predict, through Bayesian multilevel modelling, the effect of host specificity on the reproductive strategies of parasitic copepods of fishes or corals. We found that copepods of fishes with low host specificity (generalists) invest more into reproductive output with larger clutch sizes, whereas generalist copepods of corals invest less into reproductive output with smaller clutch sizes. The differences in host turnover rates through an evolutionary timescale could explain the contrasting strategies across species observed here, which should still favour the odds of parasites encountering and infecting a host. Ultimately, the differences found in this study reflect the unique evolutionary history that parasites share both intrinsically and extrinsically with their hosts.