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

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...

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Autores principales: Deppisch, Peter, Prutscher, Johanna M., Pegoraro, Mirko, Tauber, Eran, Wegener, Christian, Helfrich-Förster, Charlotte
Formato: Online Artículo Texto
Lenguaje:English
Publicado: SAGE Publications 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9008550/
https://www.ncbi.nlm.nih.gov/pubmed/35301885
http://dx.doi.org/10.1177/07487304221082448
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author Deppisch, Peter
Prutscher, Johanna M.
Pegoraro, Mirko
Tauber, Eran
Wegener, Christian
Helfrich-Förster, Charlotte
author_facet Deppisch, Peter
Prutscher, Johanna M.
Pegoraro, Mirko
Tauber, Eran
Wegener, Christian
Helfrich-Förster, Charlotte
author_sort Deppisch, Peter
collection PubMed
description 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.
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spelling pubmed-90085502022-04-15 Adaptation of Drosophila melanogaster to Long Photoperiods of High-Latitude Summers Is Facilitated by the ls-Timeless Allele Deppisch, Peter Prutscher, Johanna M. Pegoraro, Mirko Tauber, Eran Wegener, Christian Helfrich-Förster, Charlotte J Biol Rhythms Original Articles 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. SAGE Publications 2022-03-18 2022-04 /pmc/articles/PMC9008550/ /pubmed/35301885 http://dx.doi.org/10.1177/07487304221082448 Text en © 2022 The Author(s) https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution 4.0 License (https://creativecommons.org/licenses/by/4.0/) which permits any use, reproduction and distribution of the work without further permission provided the original work is attributed as specified on the SAGE and Open Access pages (https://us.sagepub.com/en-us/nam/open-access-at-sage).
spellingShingle Original Articles
Deppisch, Peter
Prutscher, Johanna M.
Pegoraro, Mirko
Tauber, Eran
Wegener, Christian
Helfrich-Förster, Charlotte
Adaptation of Drosophila melanogaster to Long Photoperiods of High-Latitude Summers Is Facilitated by the ls-Timeless Allele
title Adaptation of Drosophila melanogaster to Long Photoperiods of High-Latitude Summers Is Facilitated by the ls-Timeless Allele
title_full Adaptation of Drosophila melanogaster to Long Photoperiods of High-Latitude Summers Is Facilitated by the ls-Timeless Allele
title_fullStr Adaptation of Drosophila melanogaster to Long Photoperiods of High-Latitude Summers Is Facilitated by the ls-Timeless Allele
title_full_unstemmed Adaptation of Drosophila melanogaster to Long Photoperiods of High-Latitude Summers Is Facilitated by the ls-Timeless Allele
title_short Adaptation of Drosophila melanogaster to Long Photoperiods of High-Latitude Summers Is Facilitated by the ls-Timeless Allele
title_sort adaptation of drosophila melanogaster to long photoperiods of high-latitude summers is facilitated by the ls-timeless allele
topic Original Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9008550/
https://www.ncbi.nlm.nih.gov/pubmed/35301885
http://dx.doi.org/10.1177/07487304221082448
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