Sex differences in host defence interfere with parasite‐mediated selection for outcrossing during host–parasite coevolution

Abstract

The Red Queen hypothesis proposes that coevolving parasites select for outcrossing in the host. Outcrossing relies on males, which often show lower immune investment due to, for example, sexual selection. Here, we demonstrate that such sex differences in immunity interfere with parasite-mediated selection for outcrossing. Two independent coevolution experiments with Caenorhabditis elegans and its microparasite Bacillus thuringiensis produced decreased yet stable frequencies of outcrossing male hosts. A subsequent systematic analysis verified that male C. elegans suffered from a direct selective disadvantage under parasite pressure (i.e. lower resistance, decreased sexual activity, increased escape behaviour), which can reduce outcrossing and thus male frequencies. At the same time, males offered an indirect selective benefit, because male-mediated outcrossing increased offspring resistance, thus favouring male persistence in the evolving populations. As sex differences in immunity are widespread, such interference of opposing selective constraints is likely of central importance during host adaptation to a coevolving parasite.

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

“…However, Masri et al. (2013) demonstrated a short‐term advantage of outcrossing that supports the Red Queen hypothesis: Offspring that resulted from outcrossing were more resistant to the parasite. Taken together, these results suggest that parasite‐mediated selection pressures have the potential to support the maintenance of host outcrossing.…”

“…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.…”

“…Our results contrast slightly with those of Masri et al. (2013), who found that lower yet stable male frequencies were maintained during coevolution between C. elegans and a different bacterial parasite, B. thuringiensis . Male hosts were less resistant to the parasite and exhibited decreased sexual activity and increased escape behavior during exposure to the parasite.…”

“…Masri et al. (2013) did not find elevated host outcrossing rates during 48 generations of coevolution between C. elegans and the pathogenic bacterium Bacillus thuringiensis ; nonetheless, their results still supported the Red Queen hypothesis. Although males were more susceptible to the parasite, outcrossing was maintained throughout the experiment and outcrossed offspring exhibited stronger resistance to the parasite.…”

“…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). …”