“Periodic, parasite-mediated selection for and against sex”

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Amanda K. Gibson, Lynda F. Delph, Daniela Vergara, and Curtis M. Lively (Nov 2018)

The DOI will be https://dx.doi.org/10.1086/699829

Coevolving parasites drive fluctuations in the fitness of asexual reproduction: a long-term field and experimental study

Parasites select for and against sex

Lake Alexandrina, a waterfowl preserve located in the Mackenzie Basin on New Zealand’s South Island. Godley Peaks lies in the distance, at the north end of the lake. This photo was taken in February 2016 by Amanda K. Gibson.

Sexual reproduction isn’t an efficient way to make offspring, because males do not give birth. To make the most grandchildren, an individual female should, theoretically, clone herself. Why then is sexual reproduction such a common reproductive strategy? The Red Queen hypothesis suggests that parasites periodically give sexual females an advantage over clonal females. This study supports the Red Queen hypothesis: long-term field and experimental data indicate that parasites drive fluctuations in the fitness and frequency of clones.

These long-term field data revealed dramatic variation in the infection rate of asexual females at Lake Alexandrina: in the early 2000s, asexual females were substantially more infected by a sterilizing trematode (Microphallus) than were sexual females. By 2012, asexual females had declined in frequency and become substantially less infected than sexual females. In contrast to the wide variation in asexual infection, the infection rate of sexual females remained steady over the years.

Curt Lively snorkels through the shallows of Lake Alexandrina, collecting snails for the study. This photo was taken in January 2016 by Amanda K. Gibson.

The researchers predicted that these rare asexual females should begin to increase in frequency, because (1) asexuals can make more grand-offspring than sexuals and (2) they were less infected than the sexuals. If asexual females did not increase in frequency, the authors would reject the Red Queen hypothesis, because some force other than parasites must be preventing asexuals from outcompeting sexuals. In support of the prediction, asexual females nearly tripled in frequency at Lake Alexandrina from 2012 to 2016. The researchers ran a parallel experiment in freshwater tanks, where they allowed sexual and asexual snails from Lake Alexandrina to compete with one another in a simplified environment that isolated the effect of parasites. Asexual females also increased in frequency in these tanks. The fact that the researchers saw similar results in the field and the tanks argues that parasites contributed to the changes in asexual frequency in the field.

Amanda Gibson has just added snails from Lake Alexandrina to these freshwater tanks outside the Edward Percival Field Station in Kaikoura, New Zealand. The idea was to test if the changes in asexual frequency in the lake matched those in the controlled tank environment. The only selective force acting in the tanks was parasites. A match between lake and tank dynamics would therefore support a role for parasites in driving the evolutionary change observed in the lake. Curt Lively took this photo on January 29, 2015, when the researchers initiated the final yearly replication of the experiment.
(Credit: Curt Lively)

These results show periodic selection both for and against sex. The study demonstrates the need for long-term field data in studying host-parasite coevolution and the Red Queen. Single snapshots in time would present a misleading, simplified picture of parasite-mediated selection on reproductive mode. In keeping with this lesson, the researchers continue to follow the ongoings at Lake Alexandrina – they predict that the local parasites will begin to heavily infect asexuals again as asexual females increase in frequency.


Asexual lineages should rapidly replace sexual populations. 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. 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. 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. In the early 2000s, asexuals were more infected than sexuals. A decade later, the asexuals had declined in frequency and were less infected than sexuals. Over time, the mean infection prevalence of asexuals equaled that of sexuals, but varied far more. This variation in asexual infection prevalence suggests the potential for parasite-mediated fluctuations in asexual fitness. 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. 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. antipodarum.