Shifted levels of sleep and activity under darkness as mechanisms underlying ectoparasite resistance

Parasites harm host fitness and are pervasive agents of natural selection to evolve host defense strategies Host defensive traits in natural populations typically show genetic variation, which may be maintained when parasite resistance imposes fitness costs on the host in the absence of parasites. Previously we demonstrated significant evolutionary responses to artificial selection for increasing behavioral immunity to Gamasodes queenslandicus mites in replicate lines of Drosophila melanogaster. Here, we report transcriptional shifts in metabolic processes between selected and control fly lines based on RNA-seq analyses. We also show decreased starvation resistance and increased use of nutrient reserves in flies from mite-resistant lines. Additionally, mite-resistant lines exhibited increased behavioral activity, such as, reduced sleep and elevated oxygen consumption under conditions of darkness. The link between resistance and sleep was confirmed in an independent panel of D. melanogaster genetic lines exhibiting variable sleep durations, showing a positive correlation between mite resistance and reduced sleep. Experimentally restraining the activity of artificially selected mite-resistant flies during exposure to parasites under dark conditions reduced their resistance advantage relative to control flies. The results suggest that ectoparasite resistance in this system involves increased dark-condition activity and metabolic gene expression at the expense of nutrient reserves and starvation resistance.