Parasite-induced change in host behavior of a freshwater snail: parasitic manipulation or byproduct of infection?

Levri, Edward P.

doi:10.1093/beheco/10.3.234

Cited by 67 publications

(57 citation statements)

References 19 publications

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“…Hosts respond to parasitization with multiple phenotypic changes that serve to enhance resistance or tolerance and to decrease transmission rates. As many of these responses are unspecific and target large classes of parasites, they might coincidentally favor the transmission of one or a few specific parasites (Levri, 1999). These changes are under the genetic control of the host and, thus, cannot be considered a manipulation by the parasite in question.…”

Section: Future Stepsmentioning

confidence: 99%

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

Heil

2016

Front. Ecol. Evol.

109

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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.

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Section: Future Stepsmentioning

confidence: 99%

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

Heil

2016

Front. Ecol. Evol.

109

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“…This combination of attributes has rendered P. antipodarum an ideal model on which to test hypotheses of life history theory (e.g., Lively 1987;Jacobsen & Forbes 1997;Levri 1999;Negovetic & Jokela 2001). In this context, shell morphology has been investigated most rigorously.…”

Section: Introductionmentioning

confidence: 99%

Clinal variation in shell morphology of the freshwater gastropodPotamopyrgus antipodarumalong two hill‐country streams in New Zealand

Haase¹

2003

Journal of the Royal Society of New Zealand

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The extremely polymorphic gastropod Potamopyrgus antipodarum is widespread in freshwater habitats throughout New Zealand. This study describes morphological variation of P. antipodarum along two streams in Waikato (North Island, New Zealand), and explores relationships between morphology and selected environmental variables (temperature, conductivity, pH, flow, shade, vegetation). Along each stream, fully grown snails were collected at 11 sites extending from the source of flow to 1 or 1.5 km downstream. In both streams, shells increased in size and in one stream they also became more obese with distance from the source. Of the environmental variables assessed only flow, which increased downstream, was found to have potential influence on shell morphology. Larger snails have a larger foot and thus a larger attachment area and therefore may be able to withstand higher currents, despite having a higher Reynolds number resulting in increased drag on them relative to smaller individuals. Other studies have found that clines of morphological variation in lakes are apparently driven by the differential risk of infection by parasites. This can be excluded for the stream populations in this study, because parasitised individuals were absent at upstream sites, suggesting that similar morphological patterns may have entirely different causes.

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“…Host manipulation by parasites in snail-trematode interactions have been verified in the relationship between the New Zealand mud snail Potamopyrgus antipodarum (Gray) and the trematode Microphallus sp. (Digenea: Microphallidae) (Levri, 1999;Levri et al, 2007). The behavioural changes in P. antipodarum caused by Microphallus sp.…”

Section: Discussionmentioning

confidence: 99%

“…Many trematode parasites reduce the reproductive output of their snail hosts (parasitic castration) Rau, 1998, 1999), affect the growth of the parasitized individuals (gigantism) (Ballabeni, 1995), cause deformation of shells of the snails (Ż bikowska and Ż bikowski, 2005) and alter the biological rhythms, foraging behaviour and responses to abiotic stimuli such as light and gravity of the infected hosts (Levri, 1999;Levri and Fisher, 2000;Levri et al, 2007). Some trophically transmitted parasites are even able to alter the behaviour of their snail hosts to enhance the success of transmission to their next intermediate or definitive hosts (e.g., Levri et al, 2007).…”

Section: Introductionmentioning

confidence: 99%

Interactive effects of predation risk and parasitism on the circadian rhythm of foraging activity in the great pond snailLymnaea stagnalis(Gastropoda: Lymnaeidae)

Voutilainen

2010

Ann. Limnol. - Int. J. Lim.

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-Four experiments were serially carried out conducted to study foraging activity in the freshwater gastropod Lymnaea stagnalis in the absence and presence of predators (crayfish or fish) under daylight and in the dark. The snails were either parasitized by digenean trematodes (Diplostomum pseudospathaceum or Plagiorchis elegans) or remained unparasitized. The snails had an evident circadian foraging rhythm: they preferred diurnal foraging notwithstanding the predators and parasites. However, the snail's parasite status and the predation risk had an interaction effect on the number of feeding events per snail individual so that especially the snails parasitized by D. pseudospathaceum were more active in the presence of a fish predator than in the absence of predators. Some of the snails responded to cues from a crayfish predator by crawling out of the water. The results suggest that D. pseudospathaceum may be capable of manipulating the behaviour of its first intermediate snail host in ways that enhance its success of transmission to the parasite's second intermediate fish host. The results also indicate that the effects of biotic stressors, such as predation risk and parasitism, on the foraging pattern in the snails L. stagnalis may be interactive and highly specialized rather than generalized.

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Parasite-induced change in host behavior of a freshwater snail: parasitic manipulation or byproduct of infection?

Cited by 67 publications

References 19 publications

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

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

Clinal variation in shell morphology of the freshwater gastropodPotamopyrgus antipodarumalong two hill‐country streams in New Zealand

Interactive effects of predation risk and parasitism on the circadian rhythm of foraging activity in the great pond snailLymnaea stagnalis(Gastropoda: Lymnaeidae)

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