Rare asexual mutants should thus rapidly increase in frequency, driving sexual lineages extinct in populations where sexual and asexual lineages initially coexisted ( Maynard Smith 1971 Maynard Smith 1978). This investment in sons can reduce the per-capita birth rate of a sexual lineage by one-half relative to that of an asexual lineage (the two-fold cost of males). Sexual females produce male offspring, while asexual females do not. Sexual reproduction is not an efficient strategy. The match between field and experiment argues that coevolving parasites drive temporal change in the relative fitness and frequency of asexuals, potentially promoting the coexistence of reproductive modes in P.

Accordingly, we detected fitness consequences of the shift in parasite selection: when they were less infected than sexuals, asexuals increased in frequency in the field and in paired mesocosms that isolated the effect of parasites. This variation in asexual infection prevalence suggests the potential for parasite-mediated fluctuations in asexual fitness. Over time, the mean infection prevalence of asexuals equaled that of sexuals, but varied far more. A decade later, the asexuals had declined in frequency and were less infected than sexuals. In the early 2000’s, asexuals were more infected than sexuals. Does shifting selection by parasites drive fluctuations in the fitness and frequency of asexuals in nature? Combining long-term field data with mesocosm experiments, we detected a shift in the direction of parasite selection in the snail Potamopyrgus antipodarum and its coevolving parasite Microphallus sp. Under the Red Queen, fluctuations in parasite-mediated selection can drive fluctuations in the asexual population, leading to the coexistence of sexual and asexual reproduction. Why sex then? The Red Queen hypothesis proposes that parasite-mediated selection against common host genotypes could counteract the per-capita birth rate advantage of asexuals. Asexual lineages should rapidly replace sexual populations.

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