An experimental approach to the immuno-modulatory basis of host-parasite local adaptation in tapeworm-infected sticklebacks

Hamley, Madeleine; Franke, Frederik; Kurtz, Joachim; Scharsack, Jörn P.

doi:10.1016/j.exppara.2017.03.004

Cited by 10 publications

(16 citation statements)

References 63 publications

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“…Stickleback populations vary in resistance to S. solidus, some resistant populations defend themselves from the parasite more often (Kalbe et al 2016, Weber et al 2017a) and if infected, constrain parasite growth more efficiently than sticklebacks from susceptible populations (Kalbe et al 2016, Hamley et al 2017, Weber et al 2017b. It was suggested that acquired immune activity constrains S. solidus growth (Kurtz et al 2004), but innate immune traits, such as frequencies and respiratory burst activity of granulocytes, was correlated to variation in S. solidus resistance across stickleback populations (Hamley et al 2017, Weber et al 2017b). In combination, previous and present findings suggest that both cold temperature and immunity constrain S. solidus growth in concert.…”

Section: Discussionmentioning

confidence: 99%

Consequences of divergent temperature optima in a host–parasite system

Franke

Raifarth

Kurtz

et al. 2019

Oikos

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It was suggested that parasite infections become more severe with rising temperature, as expected during global warming. In ectothermic systems, the growth of a parasite and therefore its reproductive capacity is expected to increase with temperature. However, the outcome of the interaction depends on the temperature optima of both host and parasite. Here we used experimental infections of three‐spined stickleback fish Gasterosteus aculeatus with its specific tapeworm parasite Schistocephalus solidus to investigate in detail the temperature optima for both host and parasite. We analyzed the fitness consequences thereof, focusing on growth and immunity of the host, and growth and offspring production of the parasite as fitness correlates. We checked for potential differences among populations, using the offspring of hosts and parasites derived from four study sites in Iceland, Germany and Spain that differ in average annual temperature ranging between 4.8°C and 18.4°C. We found differences in temperature optima of host and parasites that were quite consistent across the populations: while sticklebacks grew faster and had higher immune activity at low temperatures, the parasites did not even grow fast enough to reach sexual maturity in these conditions. By contrast, with increasing temperatures, parasite growth, egg production and offspring hatching increased strongly while host immunity and growth were impaired. Our results show that divergent temperature optima of hosts and parasites can have drastic fitness consequences and support the expectation that some parasites will benefit from global warming.

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Section: Discussionmentioning

confidence: 99%

Consequences of divergent temperature optima in a host–parasite system

Franke

Raifarth

Kurtz

et al. 2019

Oikos

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“…The interaction between S. solidus and the threespine stickleback is highly specific, since it is the only fish host that this parasite can infect and it dies rapidly when ingested by other fish species (37). S. solidus infects freshwater sticklebacks (24, 38) and a combination of studies of wild populations and of experimental reciprocal cross infection data suggests local adaptation between sympatric (“native”) host-parasite pairs (39–43). For example, in distinct host-parasite population pairs, the ratio of worm to host weight, an indicator of parasite virulence, is highly similar, suggesting an optimal virulence and local adaptation (40).…”

Section: Introductionmentioning

confidence: 99%

The secretome of a parasite alters its host’s behaviour but does not recapitulate the behavioural response to infection

Berger

Aubin‐Horth

2019

Preprint

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ABSTRACTParasites with complex life cycles have been proposed to manipulate the behaviour of their intermediate hosts to increase the probability of reaching their final host. The cause of these drastic behavioural changes could be manipulation factors released by the parasite in its environment (the secretome), but this has rarely been assessed. We studied a non-cerebral parasite, the cestode Schistocephalus solidus, and its intermediate host, the threespine stickleback (Gasterosteus aculeatus), whose response to danger becomes significantly diminished when infected. These altered behaviours appear only during late infection, when the worm is ready to reproduce in its final avian host. Sympatric host-parasite pairs show higher infection success for parasites, suggesting that the secretome effects could differ for allopatric host-parasite pairs with independent evolutionary histories. We tested the effects of secretome exposure on behaviour by using secretions from the early and late infection of S. solidus and by injecting them in healthy sticklebacks from a sympatric and allopatric population. Contrary to our prediction, secretome from late infection worms did not result in more risky behaviours, but secretome from early infection resulted in more cautious hosts, only in fish from the allopatric population. Our results suggest that the secretome of Schistocephalus solidus contains molecules that can affect host behaviour, that the causes underlying the behavioural changes in infected sticklebacks are multifactorial, and that local adaptation between host-parasite pairs may extend to the response to the parasite’s secretome content.

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“…Despite its mobile final host, the population structure of S. solidus is well structured both globally (Nishimura et al 2011) and regionally (Sprehn et al 2015). In its second specific intermediate stickleback host, S. solidus shows clear evidence of coadaptation and local adaptation to its sympatric stickleback population (Kalbe et al 2016; Scharsack et al 2016; Hamley et al 2017; Weber et al 2017). In their first intermediate copepod host, not yet infective S. solidus reduce their hosts’ activity (Hammerschmidt et al 2009; Benesh, 2010 a ; Hafer and Benesh, 2015; Hafer and Milinski, 2015) and predation susceptibility (Weinreich et al 2013).…”

Section: Introductionmentioning

confidence: 99%

Differences between populations in host manipulation by the tapewormSchistocephalus solidus– is there local adaptation?

Hafer

2017

Parasitology

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Host manipulation whereby a parasite increases its transmission to a subsequent host by altering the behaviour of its current host is very far spread. It also occurs in host-parasite systems that are widely distributed. This offers the potential for local adaptation. The tapeworm Schistocephalus solidus modifies its first intermediate copepod host's predation susceptibility to suit its own needs by reducing its activity before it becomes infective and increasing it thereafter. To investigate potential differences in host manipulation between different populations and test for potential local adaptation with regard to host manipulation, I experimentally infected hosts from two distinct populations with parasites from either population in a fully crossed design. Host manipulation differed between populations mostly once the parasite had reached infectivity. These differences in infective parasites were mostly due to differences between different parasite populations.In not yet infective parasites, however, host population also had a significant effect on host manipulation. There was no evidence of local adaptation; parasites were able to manipulate foreign and local hosts equally well. Likewise, hosts were equally poor at resisting host manipulation by local and foreign parasites.

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An experimental approach to the immuno-modulatory basis of host-parasite local adaptation in tapeworm-infected sticklebacks

Cited by 10 publications

References 63 publications

Consequences of divergent temperature optima in a host–parasite system

Consequences of divergent temperature optima in a host–parasite system

The secretome of a parasite alters its host’s behaviour but does not recapitulate the behavioural response to infection

Differences between populations in host manipulation by the tapewormSchistocephalus solidus– is there local adaptation?

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