A natural timeless polymorphism allowing circadian clock synchronization in “white nights”

Abstract

Daily temporal organisation offers a fitness advantage and is determined by an interplay between environmental rhythms and circadian clocks. While light:dark cycles robustly synchronise circadian clocks, it is not clear how animals experiencing only weak environmental cues deal with this problem. Like humans, Drosophila originate in sub-Saharan Africa and spread North up to the polar circle, experiencing long summer days or even constant light (LL). LL disrupts clock function, due to constant activation of CRYPTOCHROME, which induces degradation of the clock protein TIMELESS (TIM), but temperature cycles are able to overcome these deleterious effects of LL. We show here that for this to occur a recently evolved natural timeless allele (ls-tim) is required, encoding the less light-sensitive L-TIM in addition to S-TIM, the only form encoded by the ancient s-tim allele. We show that only ls-tim flies can synchronise their behaviour to semi-natural conditions typical for Northern European summers, suggesting that this functional gain is driving the Northward ls-tim spread.

Light triggers a network switch between circadian morning and evening oscillators controlling behaviour during daily temperature cycles

“…Mai179-GAL4, UAS-cyc DN , Clk9M-GAL4, and Clk4.1-Gal4 have been outcrossed for 5 generations to iso31 to standardize the genomic background [55]. We recently showed that only flies carrying at least one copy of the natural ls-tim allele, encoding both the light sensitive S-TIM and less light sensitive L-TIM protein [27] are able to synchronize to temperature cycles in constant light, while flies homozygous for the s-tim allele (encoding only S-TIM) cannot [27]. Therefore, all strains analyzed in this study carry at least one copy of ls-tim.…”

“…Strikingly, temperature cycles are able to overcome LL-induced arrhythmicity in flies carrying a recently evolved allele of the tim gene, called ls-tim [ 22 , 26 , 27 ]. In contrast, flies bearing the original s-tim allele behave arrhythmic during temperature cycles in LL.…”

“…This is, because the S-TIM protein (the only form of TIM encoded by s-tim flies) has a high affinity to CRY, whereas L-TIM ( ls-tim flies generate both S-TIM and L-TIM) has strongly reduced affinity to CRY and is therefore more stable in the light [ 28 ]. Consequently, in the absence of CRY, s-tim flies also behave rhythmically in LL and temperature cycles [ 27 ]. In constant light and 12 h 25°C: 12 h 16°C (LLTC, 25°C-16°C), ls-tim flies are rhythmic with a single synchronized activity peak occurring in the evening [ 26 , 27 , 29 ], while in constant darkness the same temperature cycle (DDTC) leads to a behavioral activity peak in the morning in both s-tim and ls-tim flies [ 27 ].…”

“…Consequently, in the absence of CRY, s-tim flies also behave rhythmically in LL and temperature cycles [ 27 ]. In constant light and 12 h 25°C: 12 h 16°C (LLTC, 25°C-16°C), ls-tim flies are rhythmic with a single synchronized activity peak occurring in the evening [ 26 , 27 , 29 ], while in constant darkness the same temperature cycle (DDTC) leads to a behavioral activity peak in the morning in both s-tim and ls-tim flies [ 27 ]. Hence, while temperature is used as a Zeitgeber, the presence or absence of light influences the activity phase, presumably by modulating the balance toward one dominant neuronal oscillator.…”

Behavioral rhythms are bad predictors of general organismal rhythmicity

“…Similarly, differences in clock gene expression rhythms were linked to caste-specific activity phenotypes in ants 26 . Comparisons of fly strains and species from different latitudes further indicate that behavioral rhythmicity depends on the localization of circadian core clock genes expression in the brain 32, 34 and clock gene alleles 35, 36 . Furthermore, behavioral phenotypes including arrhythmicity can also depend on the circadian clock output pathways 33 .…”