Extending the ecology of fear: Parasite-mediated sexual selection drives host response to parasites

Abstract

The ‘ecology of fear’ describes the negative effects natural enemies have on potential victims even when those victims are not consumed or infected. Although recent work has demonstrated parasites have non-consumptive effects (NCE) on potential hosts, how these effects vary within host populations is not well understood. We investigated how NCE vary based on host risk of infection and relative cost of infection by measuring the metabolic rate (MR) of naive Drosophila nigrospiracula exposed to an ectoparasite, Macrocheles subbadius. We tested two mutually exclusive hypotheses: 1) asymmetrical costs of infection drive adaptions for stronger responses to parasite exposure; or 2) asymmetrical risks of infection drive adaptions for stronger responses to parasite exposure. In this system, male flies have higher costs of infection relative to female flies due to parasite-mediated sexual selection; similarly, virgin females experience higher costs of infection relative to mated females. Risk of infection also varies among flies because mites preferentially infect female flies over males, and mites preferentially infect mated females over virgin females. Our results were compatible with the hypothesis that costs of infection drive the strength of response to mite risk. Female flies responded to parasite exposure with a 15.1% increase in MR, while exposed males showed a stronger response with a 31.3% increase in MR. Mated females increased their MR by 34.8% during mite exposure whereas virgin females experienced an increase of 61.2%. Our findings suggest that NCE of parasites can vary based on state-dependent costs of infection.