Significant heritability of anti-parasite adaptations is a typical feature of natural host populations, which is paradoxical in light of the theoretical expectation that natural selection should erode additive genetic variation for fitness-related traits. A major hypothesis for the maintenance of genetic variation for parasite resistance invokes trade-offs between resistance and other fitness-conferring traits. The present study demonstrates significant heritability for behavioral resistance against ectoparasitic mites, Gamasodes queenslandicus (Parasitidae), in a natural population of the fly, Drosophila melanogaster (Drosophilidae). Deployment of energetically expensive bursts of flight was a main mechanism of resistance against mite attack. RNA-seq and functional studies identified candidate host metabolic genes involved in resistance, consistent with the fact that flight is an energetically expensive form of defense. Among adult flies, whole-body lipid and protein reserves were reduced in ectoparasite-resistant lines relative to control lines, and consequently starvation resistance was compromised also. These results suggest antagonistic pleiotropy between host resistance and host nutrient management. We also tested for costs of resistance at the larval stage of the host life cycle under variable levels of environmental stress. Resistant lines expressed significant reductions in larva-to-adult survivorship with increasing toxic (ammonia) stress, identifying an environmentally modulated pre-adult cost of resistance. Thus, ectoparasite resistance in flies is an ecological important trait with significant evolutionary potential maintained in part by environmentally modulated costs of resistance expressed across the host life cycle. The results shed light on the genetic, physiological and behavioral components of evolutionary relevant trade-offs affecting parasite resistance.
Flight or mite? The evolutionary ecology of costly behavioral resistance to ectoparasitic mites