Conflict between parasites with different transmission strategies infecting an amphipod host

Abstract

Competition between parasites within a host can influence the evolution of parasite virulence and host resistance, but few studies examine the effects of unrelated parasites with conflicting transmission strategies infecting the same host. Vertically transmitted (VT) parasites, transmitted from mother to offspring, are in conflict with virulent, horizontally transmitted (HT) parasites, because healthy hosts are necessary to maximize VT parasite fitness. Resolution of the conflict between these parasites should lead to the evolution of one of two strategies: avoidance, or sabotage of HT parasite virulence by the VT parasite. We investigated two co-infecting parasites in the amphipod host, Gammarus roeseli: VT microsporidia have little effect on host fitness, but acanthocephala modify host behaviour, increasing the probability that the amphipod is predated by the acanthocephalan's definitive host. We found evidence for sabotage: the behavioural manipulation induced by the Acanthocephala Polymorphus minutus was weaker in hosts also infected by the microsporidia Dictyocoela sp. (roeselum) compared to hosts infected by P. minutus alone. Such conflicts may explain a significant portion of the variation generally observed in behavioural measures, and since VT parasites are ubiquitous in invertebrates, often passing undetected, conflict via transmission may be of great importance in the study of host-parasite relationships.

Altered host behaviour and brain serotonergic activity caused by acanthocephalans: evidence for specificity

“…A recent study by Haine et al (2005) showed that P. minutus-infected Gammarus roeseli exhibit altered geotactic behaviour, but when G. roeseli were found to harbour infections of P. minutus along with intracellular microsporidia infections, this behavioural alteration was 'sabotaged'-co-infected individuals exhibited unaltered, normal geotactic behaviour. However, this possibility is unlikely to explain the variation seen here, since vertically transmitted microsporidia were never found in G. pulex in Burgundy (T. Rigaud, personal communication).…”

Parasite and host assemblages: embracing the reality will improve our knowledge of parasite transmission and virulence

“…The microsporidia, which is transmitted in the eggs of the gammarid, is able to disrupt the manipulation induced by the worm. This decreases the probability of predation, which is to its own benefit, as the host will have more chance to survive and reproduce, and therefore transmit the microsporidia (Haine et al 2005). Here, the strength of the selective pressure imposed on the VTP by the HTP may explain why the microsporidia evolved to counteract acanthocephalan virulence.…”

“…Even in this case, empirical results can contradict the model predictions. Haine et al (2005) showed that a VT microsporidia can alter the behavioural modification of the host (a gammarid crustacean) induced by an acanthocephalan worm. The transmission of this worm relies on trophic transmission to a final host, and behavioural modification is known to favour this transmission by increasing the predation rate by the final host.…”

Impacts of a newly identified behaviour-altering trematode on its host amphipod: from the level of gene expression to population

“…This variation may be due to several factors. Previously it has been shown that parasite load (Thomas and Poulin, 1998), age and size of parasite (Benesh et al 2008), age of host (Poulin, 1993), infection by multiple parasite species (Cezilly et al 2000;Haine et al 2005) and seasonality (Brodeur and McNeil, 1989) can all affect the intensity of parasitic manipulation. In addition, these genes can be putatively linked to serotonin pathways.…”