Parasite virulence when the infection reduces the host immune response

Abstract

Parasite infections often induce a reduction in host immune response either because of a direct manipulation of the immune system by the parasite or because of energy depletion. Although infection-induced immunodepression can favour the establishment of the parasite within the host, a too severe immunodepression may increase the risk of infection with opportunistic pathogens, stopping the period over which the parasite can be transmitted to other hosts. Here, we explore how the risk of contracting opportunistic diseases affects the survival of the amphipod Gammarus pulex infected by the acanthocephalan Pomphorhynchus laevis. Previous work with this system has shown that upon infection, G. pulex has a substantially reduced immune response. Non-infected and P. laevis-infected hosts were maintained either in control or in micro-organism-enriched water, so as to vary the risk of encountering opportunistic pathogens. As predicted, we found that host mortality was exacerbated when infected gammarids were maintained in micro-organism-enriched water compared with clean, control water; whereas for non-infected gammarids, living in micro-organism-enriched water only moderately increased the risk of mortality. These results show that the virulence of parasites that reduce the host immune response is an environmentally sensitive trait that depends on the concomitant risk for the host of contracting opportunistic diseases. This extra source of host mortality probably represents a cost for P. laevis, and we tentatively predict that the optimal level of parasite exploitation should depend on environmental conditions.

Figure 1.

Level of immune defences in G. pulex according to the status of infection by the acanthocephalan P. laevis (NI: non-infected, n = 26; I: infected, n = 19). (a) Haemocyte number, (b) PO and (c) ProPO activity per microlitre of haemolymph. Natural log-transformed data, mean ± s.e.

Figure 2.

Survival of non-infected and P. laevis-infected G. pulex maintained in control or micro-organism-enriched water in combination with a wounding treatment (see §2 for details). Legend: status of infection (non-infected versus infected), water quality (control versus mirco-organism-enriched), wounding (non-wounded versus wounded). Open squares: non-infected, control, non-wounded. Filled squares: non-infected, micro-organism, non-wounded. Open triangles: infected, control, non-wounded. Filled triangles: infected, micro-organism, non-wounded. Asterisks: non-infected, control, wounded. Crosses: non-infected, micro-organism, wounded. Open diamonds: infected, control, wounded. Filled diamonds: infected, micro-organism, wounded.

Figure 3.

Illustration of the significant interaction ‘status of infection × water quality’ highlighted in the survival analysis model: (a) cumulative survival and (b) risk ratio (with 95% confidence interval). Square: non-infected host. Triangle: infected host. Open symbol: control water. Filled symbol: micro-organism-enriched water.

Figure 4.

Illustration of the significant interaction ‘water quality × wounding’ highlighted in the survival analysis model: (a) cumulative survival and (b) risk ratio (with 95% confidence interval). Square: non-wounded host. Triangle: wounded host. Open symbol: control water. Fixed symbol: micro-organism-enriched water.