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Keywords:

  • adaptive dynamics;
  • co-evolution;
  • evolutionary ecology;
  • host–parasite interactions;
  • Red Queen

Summary

1.  The idea that parasites can affect host diversity is pervasive, and the possibility that parasites can increase host diversity is of particular interest. In this review, we focus on diversity in the resistance of hosts to their parasites, and on the different ways in which parasites can increase or decrease this resistance diversity.

2.  Theoretically, parasites can exert many different types of selection on host populations, which each have consequences for host diversity. Specifically, theory predicts that parasites can exert negative frequency-dependent selection (NFDS) and disruptive selection on resistance, both of which increase host diversity, as well as directional selection and stabilizing selection on resistance, both of which decrease host diversity.

3.  Despite these theoretical predictions, most biologists think of only NFDS or directional selection for increased resistance in response to parasitism. Here, we present empirical support for all of these types of selection occurring in natural populations. Interestingly, several recent studies demonstrate that there is spatiotemporal variation in the type of selection that occurs (and, therefore, in the effects of parasitism on host diversity).

4.  A key question that remains, then, is: What determines the type of parasite-mediated selection that occurs? Theory demonstrates that the answer to this question lies, at least in part, with trade-offs associated with resistance. Specifically, the type of evolution that occurs depends critically on the strength and shape of these trade-offs. This, combined with empirical evidence for a strong effect of environment on the shape and strength of trade-offs, may explain the observed spatiotemporal variation in parasite-mediated selection.

5.  We conclude that spatiotemporal variation in parasite-driven evolution is likely to be common, and that this variation may be driven by ecological factors. We suggest that the feedback between ecological and evolutionary dynamics in host–parasite interactions is likely to be a productive area of research. In particular, studies addressing the role of ecological factors (e.g. productivity and predation regimes) in driving the outcome of parasite-mediated selection on host populations are warranted. Such studies are necessary if we are to understand the mechanisms underlying the observed variation in the effects of parasites on host diversity.