Larks, owls, swifts, and woodcocks among fruit flies: Differential responses of four heritable chronotypes to long and hot summer days

Abstract

Purpose: Drosophila melanogaster and our own species share (Homo sapiens) the history of relatively rapid out-of-Africa dispersal. In Eurasia, they had faced a novel adaptive problem of adjustment of their circadian rhythmicity and night sleep episode to seasonal variation in day length and air temperature. Both species usually respond to heat and a short duration of night by reduction of the amount of night sleep and prolongation of “siesta”. To further explore similarities between the two species in the ways of adjustment of their sleep–wake behavior to extreme environmental factors, this study examined the possibility to distinguish four extreme chronotypes among fruit flies and the possibility of the differential response of such chronotypes to light and heat stressors. Materials and methods: Circadian rhythms of locomotor activity and sleep–wake pattern were tested in constant darkness, and four strains of fruit flies originating from three wild populations of Africa, Europe, and the USA were selected to represent four distinct chronotypes: “larks” (early morning and evening activity peaks), “owls” (late morning and evening peaks), “swifts” (early morning and late evening peaks), and “woodcocks” (late morning and early evening peaks). The circadian rhythms and sleep efficiency of the selected chronotypes were further tested under such extreme conditions as either long day (LD20:4 at 20°C) or a combination of LD20:4 with hot temperature (29°C). Results: Despite the identity of such experimental conditions for four chronotypes, their circadian rhythms and sleep timing showed significantly distinct patterns of response to exposure to heat and/or long days. All two-way repeated measures analysis of variances yielded a significant interaction between chronotype and time of the day (P<0.001). Conclusion: An experimental study of heritable chronotypes in the fruit fly can facilitate a search for genetic underpinnings of individual variation in vulnerability to circadian misalignment, maladaptive sleep–wake behavior, and sleep disorders.