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

Abstract

Parasites harm host fitness and are pervasive agents of natural selection. Host defensive traits in natural populations typically show genetic variation, which may be maintained when parasite resistance imposes fitness costs on the host coupled with variability in parasite prevalence in space and/or time. Previously we demonstrated significant evolutionary responses to artificial selection for increasing behavioral immunity toGamasodes queenslandicusmites in replicate lines ofDrosophila 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, reduced sleep and elevated oxygen consumption under conditions of darkness. The link between resistance and sleep was confirmed in an independent panel ofD. melanogastergenetic 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.

Intra-species quantification reveals differences in activity and sleep levels in the yellow fever mosquito,Aedes aegypti

“…The activity and sleep profiles and levels of the multiple lines of Ae. aegypti were quantified using a Locomotor Activity Monitor 25 (LAM25) system developed for Drosophila (TriKinetics Inc., Waltham, MA, USA) and adapted for mosquitoes and ticks (Rund et al, 2012;Lima-Camara et al, 2014;Rosendale et al, 2019;Ajayi et al, 2022;Benoit et al, 2023). For each line, individual mosquitoes were loaded into 25×150 mm clear glass tubes with access to water and 10% sucrose provided ad libitum.…”