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Lifecycle of Dicrocoelium dendriticum. Eggs are excreted from an herbivorous mammal serving as the definitive host and hatch into a miracidium when ingested by a terrestrial snail. Mother and daughter sporocysts develop in the hepatopancreas of the snail (not shown), producing the cercaria stage. Cercariae are released from the snail via slimeballs excreted from the pneumastoma. Ants eat the slimeballs containing infective cercariae, which develop into metacercariae in the hemocoel of the gaster of the ant. However, one or more cercariae penetrates the lining of the crop upon ingestion and migrates to the suboesophageal ganglion (depicted in the headcapsule of the ant by arrow; Martín-Vega et al. 2018), where it induces a reversible biting behavior of the ants where the mandibles are locked to vegetation leaving the ant exposed to ingestion by a suitable definitive host. Following ingestion, the metacercariae excyst in the duodenum, migrate to the bile ducts of the liver and mature to become adult worms producing large numbers of eggs by sexual reproduction. Original drawing by Simone Nordstrand Gasque.
Source publication
Parasite-induced modification of host behavior increasing transmission to a next host is a common phenomenon. However, field-based studies are rare, and the role of environmental factors in eliciting host behavioral modification is often not considered. We examined the effects of temperature, relative humidity (RH), time of day, date, and an irradi...
Citations
... This behavior is considered to provide several benefits to the parasite: first, it can increase the visibility of the dying host, making it more likely to be consumed by a predator, which then acts as the next host and/or carrier/dispersal agent for the pathogen. One example is the infection of host ants by the trematode, Dicrocoelium dendriticum, where infected ants exhibit altered diurnal activities, including nocturnal climbing behavior such as ascending vegetation during the nighttime (Gasque and Fredensborg 2023). This climbing behavior increases the likelihood of predation by grazing mammals, which in turn act as the next host for the parasite, allowing for the completion of the parasite's life cycle. ...
Summit disease, in which infected hosts seek heights (gravitropism), first noted in modern times by nineteenth-century naturalists, has been shown to be induced by disparate pathogens ranging from viruses to fungi. Infection results in dramatic changes in normal activity patterns, and such parasite manipulation of host behaviors suggests a strong selection for convergent outcomes albeit evolved via widely divergent mechanisms. The two best-studied examples involve a subset of viral and fungal pathogens of insects that induce “summiting” in infected hosts. Summiting presumably functions as a means for increasing the dispersal of the pathogen, thus significantly increasing fitness. Here, we review current advances in our understanding of viral- and fungal-induced summit disease and the host behavioral manipulation involved. Viral genes implicated in this process include a host hormone-targeting ecdysteroid UDP-glucosyltransferase (apparently essential for mediating summit disease induced by some viruses but not all) and a protein tyrosine phosphatase, with light dependance implicated. For summit disease-causing fungi, though much remains obscure, targeting of molting, circadian rhythms, sleep, and responses to light patterns appear involved. Targeting of host neuronal pathways by summit-inducing fungi also appears to involve the production of effector molecules and secondary metabolites that affect host muscular, immune, and/or neurological processes. It is hypothesized that host brain structures, particularly Mushroom Bodies (no relation to the fungus itself), important for olfactory association learning and control of locomotor activity, are critical targets for mediating summiting during infection. This phenomenon expands the diversity of microbial pathogen-interactions and host dynamics.
Key points
• Summit disease or height seeking (gravitropism) results from viral and fungal pathogens manipulating insect host behaviors presumably to increase pathogen dispersal.
• Insect baculoviruses and select fungal pathogens exhibit convergent evolution in host behavioral manipulation but use disparate molecular mechanisms.
• Targets for affecting host behavior include manipulation of host hormones, feeding, locomotion, and immune, circadian, and neurological pathways.
Parasites have a rich and long natural history among biological entities, and it has been suggested that parasites are one of the most significant factors in the evolution of their hosts. However, it has been emphasized less frequently how co‐evolution has undoubtedly also shaped the paths of parasites. It may seem safe to assume that specific differences among the array of potential hosts for particular parasites have restricted and diversified their evolutionary pathways and strategies for survival. Nevertheless, if one looks closely enough at host and parasite, one finds commonalities, both in terms of host defences and parasite strategies to out‐manoeuvre them. While such analyses have been the source of numerous reviews, they are generally limited to interactions between, at most, one kingdom of parasite with two kingdoms of host (e.g. similarities in animal and plant host responses against fungi). With the aim of extending this view, we herein critically evaluate the similarities and differences across all four eukaryotic host kingdoms (plants, animals, fungi, and protists) and their parasites. In doing so, we show that hosts tend to share common strategies for defence, including both physical and behavioural barriers, and highly evolved immune responses, in particular innate immunity. Parasites have, similarly, evolved convergent strategies to counter these defences, including mechanisms of active penetration, and evading the host's innate and/or adaptive immune responses. Moreover, just as hosts have evolved behaviours to avoid parasites, many parasites have adaptations to manipulate host phenotype, physiologically, reproductively, and in terms of behaviour. Many of these strategies overlap in the host and parasite, even across wide phylogenetic expanses. That said, specific differences in host physiology and immune responses often necessitate different adaptations for parasites exploiting fundamentally different hosts. Taken together, this review facilitates hypothesis‐driven investigations of parasite–host interactions that transcend the traditional kingdom‐based research fields.
Parasite manipulation of host behavior, as an effective strategy to establish transmission, has evolved multiple times across taxa, including fungi. Major strides have been made to propose molecular mechanisms that underlie manipulative parasite-host interactions including the manipulation of carpenter ant behavior by Ophiocordyceps. This research suggests that the secretion of parasite proteins and light-driven biological rhythms are likely involved in the infection and manipulation biology of Ophiocordyceps and other manipulating parasites. Here, we discuss research on Ophiocordyceps considering findings from other (fungal) parasites that either are relatively closely related (e.g., other insect- and plant-infecting Hypocreales) or also manipulate insect behavior (e.g., Entomophthorales). As such, this review aims to put forward this question: Are the mechanisms behind Ophiocordyceps manipulation and infection unique, or did they convergently evolve? From this discussion, we pose functional hypotheses about the infection biology of Ophiocordyceps that will need to be addressed in future studies.
Neuroparasitism concerns the hostile takeover of a host's nervous system by a foreign invader, in order to alter the behaviour of the host in favour of the parasite. One of the most remarkable cases of parasite-induced host behav-ioural manipulation comprises the changes baculoviruses induce in their caterpillar hosts. Baculoviruses may manipulate caterpillar behaviour in two ways: hyperactivity (increased movement in the horizontal plane) and/or treetop disease (movement to elevated levels in the vertical plane). Those behavioural changes are followed by liquefaction and death of the caterpillar. In Autographa californica multiple nucleopolyhedrovirus (AcMNPV)-infected Spodoptera exigua caterpillars, an enzymatic active form of the virally encoded protein tyrosine phosphatase (PTP) is needed for the expression of hyperactivity from 3 days post infection (dpi). Using eGFP-expressing recombinant AcMNPV strains, we show that infection of the caterpillar's central nervous system (CNS) can be observed primarily from 3 dpi onwards. In addition, we demonstrate that the structural and enzymatic function of PTP does not play a role in infection of the CNS. Instead we show that the virus entered the CNS via the trachea, progressing caudally to frontally through the CNS and that the infection progressed from the outermost cell layers towards the inner cell layers of the CNS, in a PTP independent manner. These findings help to further understand parasitic manipulation and the mechanisms by which neuroparasites infect the host nervous system to manipulate host behaviour.
