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

Peter Deppisch, Johanna M. Prutscher, Mirko Pegoraro, Eran Tauber, Christian Wegener, Charlotte Helfrich-Förster

Research output: Contribution to journalArticlepeer-review

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.

Original languageEnglish
JournalJournal of Biological Rhythms
DOIs
StateAccepted/In press - 2022

Bibliographical note

Funding Information:
We are grateful to John Pool and Bill Ballard for collecting isofemale lines in Zambia and Zimbabwe. We thank Ralf Stanewsky for comments on our manuscript and for providing information prior to publication of their paper (Lamaze et al., 2021), the members at the Neurobiology and Genetics for fruitful discussions, Susanne Kl?hspies for help with establishing isofemale lines, and Irina Wenzel for language proof reading. This work was supported by the German Research Foundation (DFG) (grant number: FO207/15-2).

Funding Information:
We are grateful to John Pool and Bill Ballard for collecting isofemale lines in Zambia and Zimbabwe. We thank Ralf Stanewsky for comments on our manuscript and for providing information prior to publication of their paper (), the members at the Neurobiology and Genetics for fruitful discussions, Susanne Klühspies for help with establishing isofemale lines, and Irina Wenzel for language proof reading. This work was supported by the German Research Foundation (DFG) (grant number: FO207/15-2).

Publisher Copyright:
© 2022 The Author(s).

Keywords

  • arrhythmicity
  • evening peak
  • locomotor activity
  • rhythmicity
  • timeless polymorphism

ASJC Scopus subject areas

  • Physiology
  • Physiology (medical)

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