Parasitism shaping host life-history evolution: adaptive responses in a marine gastropod to infection by trematodes

In the face of continuous threats from parasites, hosts have evolved an elaborate series of preventative and controlling measures - the immune system - in order to reduce the fitness costs of parasitism. However, these measures do have associated costs. Viewing an individual's immune response to parasites as being subject to optimization in the face of other demands offers potential insights into mechanisms of life history trade-offs, sexual selection, parasite-mediated selection and population dynamics. We discuss some recent results that have been obtained by practitioners of this approach in natural and semi-natural populations, and suggest some ways in which this field may progress in the near future.

Recent interest has focused on immune response in an evolutionary context, with particular attention to disease resistance as a life-history trait, subject to trade-offs against other traits such as reproductive effort. Immune defense has several characteristics that complicate this approach, however; for example, because of the risk of autoimmunity, optimal immune defense is not necessarily maximum immune defense. Two important types of cost associated with immunity in the context of life history are resource costs, those related to the allocation of essential but limited resources, such as energy or nutrients, and option costs, those paid not in the currency of resources but in functional or structural components of the organism. Resource and option costs are likely to apply to different aspects of resistance. Recent investigations into possible trade-offs between reproductive effort, particularly sexual displays, and immunity have suggested interesting functional links between the two. Although all organisms balance the costs of immune defense against the requirements of reproduction, this balance works out differently for males than it does for females, creating sex differences in immune response that in turn are related to ecological factors such as the mating system. We conclude that immune response is indeed costly and that future work would do well to include invertebrates, which have sometimes been neglected in studies of the ecology of immune defense.

The extent to which an organism is selected to invest in defences against pathogens and parasites depends on the advantages that ensue should infection occur, but also on the costs of maintaining defences in the absence of infection. The presence of heritable variation in resistance suggests that costs exist, but we know very little about the nature or magnitude of these costs in natural populations of animals. A powerful technique for identifying trade-offs between fitness components is the study of correlated responses to artificial selection. We have selected Drosophila melanogaster for improved resistance against an endoparasitoid, Asobara tabida. Endoparasitoids are insects whose larvae develop internally within the body of other insects, eventually killing them, although their hosts can sometimes survive attack by mounting a cellular immune response. We found that reduced larval competitive ability in unparasitized D. melanogaster is a correlated response to artificial selection for improved resistance against A. tabida. The strength of selection for competitive ability and parasitoid resistance is likely to vary temporally and spatially, which may explain the observed heritable variation in resistance.