Adaptation of Drosophila melanogaster to Long Photoperiods of High-Latitude Summers Is Facilitated by the ls-Timeless Allele

Author:

Deppisch Peter1,Prutscher Johanna M.1,Pegoraro Mirko2,Tauber Eran3,Wegener Christian1,Helfrich-Förster Charlotte1

Affiliation:

1. Neurobiology and Genetics, Theodor-Boveri Institute, Biocenter, Julius-Maximilians-University of Würzburg, Würzburg, Germany

2. Faculty of Science, School of Biological and Environmental Science, Liverpool John Moores University, Liverpool, UK

3. Department of Evolutionary and Environmental Biology, Institute of Evolution, University of Haifa, Haifa, Israel

Abstract

Circadian clocks help animals to be active at the optimal time of the day whereby for most species the daily light-dark cycle is the most important zeitgeber for their circadian clock. In this respect, long arctic summer days are particularly challenging as light is present almost 24 h per day, and continuous light makes the circadian clocks of many animals arrhythmic. This is especially true for the fruit fly, Drosophila melanogaster, which possesses a very light-sensitive clock. The blue-light photoreceptor Cryptochrome (CRY) and the clock protein Timeless (TIM) are the light-sensitive components of the circadian clock and are responsible for constant light-induced arrhythmicity even at very low light intensities. Nevertheless, D. melanogaster was able to spread from its tropical origin and invade northern latitudes. Here, we tested whether a natural polymorphism at the timeless ( tim) locus, s-tim and ls-tim, helped adaptation to very long photoperiods. The recently evolved natural allele, ls-tim, encodes a longer, less light sensitive form of TIM (L-TIM) in addition to the shorter (S-TIM) form, the only form encoded by the ancient s-tim allele. ls-tim has evolved in southeastern Italy and slowly spreads to higher latitudes. L-TIM is known to interact less efficiently with CRY as compared with S-TIM. Here, we studied the locomotor activity patterns of ~40 wild s-tim and ls-tim isofemale lines caught at different latitudes under simulated high-latitude summer light conditions (continuous light or long photoperiods with 20-h daily light). We found that the ls-tim lines were significantly more rhythmic under continuous light than the s-tim lines. Importantly, the ls-tim lines can delay their evening activity under long photoperiods, a behavioral adaptation that appears to be optimal under high-latitude conditions. Our observations suggest that the functional gain associated with ls-tim may drive the northern spread of this allele by directional selection.

Publisher

SAGE Publications

Subject

Physiology (medical),Physiology

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