Infection Dynamics in Coexisting Sexual and Asexual Host Populations: Support for the Red Queen Hypothesis

Abstract

The persistence of sexual reproduction is a classic problem in evolutionary biology. The problem stems from the fact that, all else equal, asexual lineages should rapidly replace coexisting sexual individuals due to the cost of producing males in sexual populations. One possible countervailing advantage to sexual reproduction is that, on average, outcrossed offspring are more resistant than common clones to coevolving parasites, as predicted under the Red Queen hypothesis. In this study, we evaluated the prevalence of infection by a sterilizing trematode (Microphallus sp.) in a natural population of freshwater snails that was composed of both sexual and asexual individuals (Potamopyrgus antipodarum). More specifically, we compared the frequency of infection in sexual and asexual individuals over a 5-year period at four sites at a natural glacial lake (Lake Alexandrina, South Island, New Zealand). We found that at most sites and over most years, the sexual population was less infected than the coexisting asexual population. Moreover, the frequency of uninfected sexual females was periodically greater than two times the frequency of uninfected asexual females. These results give clear support for a fluctuating parasite-mediated advantage to sexual reproduction in a natural population.

Fine-scale association between parasites and sex in Potamopyrgus antipodarum within a New Zealand lake

“…The association remained when the infection rates of females only were used (ρ = 0.643, p = 0.004), demonstrating that this parasite-sex connection was not driven by potential differences in susceptibility between males and females (also see Vergara et al 2014). We also detected a significant positive correlation between the frequency of Microphallus infection alone and the relative frequency of males (ρ = 0.535, p = 0.022).…”

“…We performed this second Spearman analysis because Microphallus in particular has been implicated as a likely player in the maintenance of sexual reproduction in many previous P. antipodarum studies (e.g. Lively 1987;Jokela et al 2009;Vergara et al 2014).…”

“…Nearly all of these within-lake studies have focused on Lake Alexandrina (MacKenzie District, Canterbury, South Island; e.g. Jokela & Lively 1995a, b;Paczesniak et al 2014;Vergara et al 2014); whether the patterns uncovered in Lake Alexandrina are broadly generalizable to other New Zealand lakes remains unclear.…”

Turnover in local parasite populations temporarily favors host outcrossing over self‐fertilization during experimental evolution

“…Host–parasite coevolution can generate the constantly shifting adaptive landscapes that are likely necessary for the long‐term maintenance of outcrossing, as shown in natural populations (Jokela et al., 2009; Vergara et al., 2014) and experimental systems (Masri et al., 2013; Morran et al., 2011). While other mechanisms may be capable of producing similar dynamics, it remains to be determined whether selective pressures apart from host–parasite coevolution can drive the long‐term maintenance of outcrossing.…”

“…Conversely, self‐fertilizing hosts are more likely to produce offspring with common genotypes that are predicted to suffer disproportionately from parasite infection. The fitness advantage that outcrossed offspring gain from reduced parasitism can fluctuate over time; if this advantage periodically outweighs the costs of sex, then outcrossing will be maintained in the long term (Vergara, Jokela, & Lively, 2014). Many studies of natural and experimental host–parasite coevolution have provided support for the Red Queen hypothesis (Dybdahl & Lively, 1998; Jokela, Dybdahl, & Lively, 2009; King, Delph, Jokela, & Lively, 2009; Koskella & Lively, 2009; Lively & Dybdahl, 2000; Masri et al., 2013; Morran, Schmidt, Gelarden, Parrish, & Lively, 2011; Slowinski et al., 2016; Vergara et al., 2014).…”