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Abstract Our understanding of the evolutionary significance of ectoparasites in natural communities is limited by a paucity of information concerning the mechanisms and heritability of resistance to this ubiquitous group of organisms. Here, we report the results of artificial selection for increasing ectoparasite resistance in replicate lines of Drosophila melanogaster derived from a field-fresh population. Resistance, as ability to avoid infestation by naturally co-occurring Gamasodes queenslandicus mites, increased significantly in response to selection and realized heritability (SE) was estimated to be 0.11 (0.0090). Deployment of energetically expensive bursts of flight from the substrate was a main mechanism of host resistance that responded to selection, aligning with previously documented metabolic costs of fly behavioral defenses. Host body size, which affects parasitism rate in some fly–mite systems, was not shifted by selection. In contrast, resistant lines expressed significant reductions in larva-to-adult survivorship with increasing toxic (ammonia) stress, identifying an environmentally modulated preadult cost of resistance. Flies selected for resistance to G. queenslandicus were also more resistant to a different mite, Macrocheles subbadius, suggesting that we documented genetic variation and a pleiotropic cost of broad-spectrum behavioral immunity against ectoparasites. The results demonstrate significant evolutionary potential of resistance to an ecologically important class of parasites. 

Traumatic insemination (TI) is a rare reproductive behaviour characterized by the transfer of sperm to the female via puncture wounds inflicted across her body wall. Here, we challenge the claim made by Kamimura (Kamimura 2007 Biol. Lett. 3 , 401–404. ( doi:10.1098/rsbl.2007.0192 )) that males of species of the Drosophila bipectinata complex use a pair of claw-like processes (claws) to traumatically inseminate females: the claws are purported to puncture the female body wall and genital tract, and to inject sperm through the wounds into the lumen of her genital tract, bypassing the vaginal opening. This supposed case of TI is widely cited and featured in prominent subject reviews. We examined high-resolution scanning electron micrographs of the claws and failed to discover any obvious ‘groove’ for sperm transport. We demonstrated that sperm occurred in the female reproductive tract as a single-integrated unit, inconsistent with the claim that sperm are injected via paired processes. Laser ablation of the sharp terminal ends of the claws failed to inhibit insemination. We showed that the aedeagus in the complex delivers sperm through the vaginal opening, as in other Drosophila . The results refute the claim of TI in the Drosophila bipectinata species complex. 

Abstract Parasites cause harm to their hosts and represent pervasive causal agents of natural selection. Understanding host proximate responses during interactions with parasites can help predict which genes and molecular pathways are targets of this selection. In the current study, we examined transcriptional changes arising from interactions between Drosophila melanogaster and their naturally occurring ectoparasitic mite, Gamasodes queenslandicus . Shifts in host transcript levels associated with behavioural avoidance revealed the involvement of genes underlying nutrient metabolism. These genetic responses were reflected in altered body lipid and glycogen levels in the flies. Mite infestation triggered a striking immune response, while male accessory gland protein transcript levels were simultaneously reduced, suggesting a trade-off between host immune responses to parasite challenge and reproduction. Comparison of transcriptional analyses during mite infestation to those during nematode and parasitoid attack identified host genes similarly expressed in flies during these interactions. Validation of the involvement of specific genes with RNA interference lines revealed candidates that may directly mediate fly–ectoparasite interactions. Our physiological and molecular characterization of the Drosophila – Gamasodes interface reveals new proximate mechanisms underlying host–parasite interactions, specifically host transcriptional shifts associated with behavioural avoidance and infestation. The results identify potential general mechanisms underlying host resistance and evolutionarily relevant trade-offs.