In Search of the Red Queen: A Response

The Comment by Woolhouse and Webster (this issue) makes several valid points. For example, the authors indicate that, because of time lags, the most common host genotypes might sometimes be overinfected and sometimes be underinfected. We agree 1xHost–parasite interactions: infection of common clones in natural populations of a freshwater snail (Potamopyrgus antipodarum). Dybdahl, M.F. and Lively, C.M. Proc. R. Soc. London B Biol. Sci. 1995; 260: 99–103CrossrefSee all References. Our awareness of the complications imposed by time lags is the reason we focused on the host population (in Lake Poerua, New Zealand) for which we knew the identity of clones over time, thereby allowing us to pick out the clones that had been common in the recent past 2xParasite adaptation to locally common host genotypes. Lively, C.M. and Dybdahl, M.F. Nature. 2000; 405: 679–681Crossref | PubMed | Scopus (316)See all References. We were interested primarily in whether these recently common clones (RCCs) would become more infected in our experiment than would rare clones, independent of parasite source (the trade-off hypothesis); or whether overinfection of RCCs would be restricted to the sympatric source of parasites (the co-evolution hypothesis).Woolhouse and Webster suggest that our statistical analysis of this experiment was inadequate, because we did not test for an interaction between host genotype and parasite origin. The interaction they seek, between infection, host genotype (common vs rare), and parasite source (sympatric, allopatric and mixed), was highly significant (Likelihood Ratio χ2=10.637; df=3; p=0.0049). Underlying this effect is our result that common clones were more infected than were rare clones by the sympatric source of parasites, but there were no overall differences in infection for rare vs common clones in either the allopatric or the mixed sources of parasites 2xParasite adaptation to locally common host genotypes. Lively, C.M. and Dybdahl, M.F. Nature. 2000; 405: 679–681Crossref | PubMed | Scopus (316)See all References. One isolated exception to the general pattern was RCC 22, which was more infected than were the rare clones by the allopatric parasite source (χ2=7.18, df=1; p=0.007); but the same clone was not more infected in the mixed source of parasites (χ2=0.78, df=1; p=0.378). Hence, there is no evidence that this particular common clone is inherently more susceptible to infection. Similarly, there is no evidence that any of the other three RCCs were inherently more susceptible to infection than were the rare clones, as required by the trade-off hypothesis 2xParasite adaptation to locally common host genotypes. Lively, C.M. and Dybdahl, M.F. Nature. 2000; 405: 679–681Crossref | PubMed | Scopus (316)See all References. This finding does not eliminate the possibility of costs of resistance; but it does suggest that these costs (if present) do not account for the overinfection of common clones by the local parasite source 2xParasite adaptation to locally common host genotypes. Lively, C.M. and Dybdahl, M.F. Nature. 2000; 405: 679–681Crossref | PubMed | Scopus (316)See all References.Woolhouse and Webster suggest that our design could, at best, provide only weak evidence for local adaptation, because we used only one source of target snails. However, our evidence for local adaptation comes from three reciprocal crossinfection experiments: two experiments involving four populations in 1987 (3xAdaptation by a parasitic trematode to local populations of its snail host. Lively, C.M. Evolution. 1989; 43: 1663–1671CrossrefSee all References), and one experiment involving two populations in 1997 (2xParasite adaptation to locally common host genotypes. Lively, C.M. and Dybdahl, M.F. Nature. 2000; 405: 679–681Crossref | PubMed | Scopus (316)See all References). In all six populations, the parasites were more infective to local hosts. Nonetheless, we accept that we had only host source in our experimental test of the trade-off and co-evolution models. More experiments of this kind would be welcome, but we note that our experiment could have easily falsified the co-evolution model. All that was required was either: (1) no difference in infection between RCCs and rare clones in the sympatric parasite source; or (2) RCCs were more infected, independent of parasite source.Along these lines, Woolhouse and Webster suggest that the Red Queen hypothesis would be hard to test by experiments that investigate only geographic patterns. Our feeling is that it would be impossible to prove the existence of the Red Queen using only reciprocal crossinfection experiments, but easy to falsify. We would have abandoned the idea if these parasites had shown no local adaptation on some spatial scale. But we agree that the search for the Red Queen is far from over. Hopefully, many creative tests and exciting ideas will emerge during this search, whether or not the Red Queen eventually proves to be a useful model.We thank Mark Woolhouse, Andy Peters, Jukka Jokela and Joanne Webster for constructive comments, and Lynda Delph for advice concerning log-linear models.