Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.

Subscribe

Logo for

Science 316 (5833): 1895-1898

Copyright © 2007 by the American Association for the Advancement of Science

Natural Selection Favors a Newly Derived timeless Allele in Drosophila melanogaster

Eran Tauber,1* Mauro Zordan,2* Federica Sandrelli,2* Mirko Pegoraro,1,2 Nicolò Osterwalder,2 Carlo Breda,1,2 Andrea Daga,2{dagger} Alessandro Selmin,1,2 Karen Monger,1 Clara Benna,2 Ezio Rosato,1 Charalambos P. Kyriacou,1{ddagger} Rodolfo Costa2

Abstract: Circadian and other natural clock-like endogenous rhythms may have evolved to anticipate regular temporal changes in the environment. We report that a mutation in the circadian clock gene timeless in Drosophila melanogaster has arisen and spread by natural selection relatively recently in Europe. We found that, when introduced into different genetic backgrounds, natural and artificial alleles of the timeless gene affect the incidence of diapause in response to changes in light and temperature. The natural mutant allele alters an important life history trait that may enhance the fly's adaptation to seasonal conditions.

1 Department of Genetics, University of Leicester, Leicester LE1 7RH, UK.
2 Department of Biology, University of Padova, 35131 Padova, Italy.

* These authors contributed equally to this work.

{dagger} Present address: Department of Pharmacology, University of Padova, Largo Meneghetti 2, 35131 Padova, Italy.

{ddagger} To whom correspondence should be addressed. E-mail: cpk{at}leicester.ac.uk


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Clock Gene Evolution: Seasonal Timing, Phylogenetic Signal, or Functional Constraint?.
T. J. Krabbenhoft and T. F. Turner (2014)
J. Hered. 105, 407-415
   Abstract »    Full Text »    PDF »
Moonlight Detection by Drosophila's Endogenous Clock Depends on Multiple Photopigments in the Compound Eyes.
M. Schlichting, R. Grebler, N. Peschel, T. Yoshii, and C. Helfrich-Forster (2014)
J Biol Rhythms 29, 75-86
   Abstract »    Full Text »    PDF »
Animal activity around the clock with no overt circadian rhythms: patterns, mechanisms and adaptive value.
G. Bloch, B. M. Barnes, M. P. Gerkema, and B. Helm (2013)
Proc R Soc B 280, 20130019
   Abstract »    Full Text »    PDF »
Latitudinal clines: an evolutionary view on biological rhythms.
R. A. Hut, S. Paolucci, R. Dor, C. P. Kyriacou, and S. Daan (2013)
Proc R Soc B 280, 20130433
   Abstract »    Full Text »    PDF »
Evolutionary Links Between Circadian Clocks and Photoperiodic Diapause in Insects.
M. E. Meuti and D. L. Denlinger (2013)
Integr. Comp. Biol. 53, 131-143
   Abstract »    Full Text »    PDF »
Clocks for the city: circadian differences between forest and city songbirds.
D. M. Dominoni, B. Helm, M. Lehmann, H. B. Dowse, and J. Partecke (2013)
Proc R Soc B 280, 20130593
   Abstract »    Full Text »    PDF »
Autonomous regulation of the insect gut by circadian genes acting downstream of juvenile hormone signaling.
A. Bajgar, M. Jindra, and D. Dolezel (2013)
PNAS 110, 4416-4421
   Abstract »    Full Text »    PDF »
Drosophila Clock Neurons under Natural Conditions.
P. Menegazzi, S. Vanin, T. Yoshii, D. Rieger, C. Hermann, V. Dusik, C. P. Kyriacou, C. Helfrich-Forster, and R. Costa (2013)
J Biol Rhythms 28, 3-14
   Abstract »    Full Text »    PDF »
Laboratory versus Nature: The Two Sides of the Drosophila Circadian Clock.
P. Menegazzi, T. Yoshii, and C. Helfrich-Forster (2012)
J Biol Rhythms 27, 433-442
   Abstract »    Full Text »    PDF »
Extreme Conservation and Non-Neutral Evolution of the cpmA Circadian Locus in a Globally Distributed Chroococcidiopsis sp. from Naturally Stressful Habitats.
V. Dvornyk and A. S. Jahan (2012)
Mol. Biol. Evol. 29, 3899-3907
   Abstract »    Full Text »    PDF »
Flies in the North: Locomotor Behavior and Clock Neuron Organization of Drosophila montana.
H. Kauranen, P. Menegazzi, R. Costa, C. Helfrich-Forster, A. Kankainen, and A. Hoikkala (2012)
J Biol Rhythms 27, 377-387
   Abstract »    Full Text »    PDF »
A Critical Assessment of Storytelling: Gene Ontology Categories and the Importance of Validating Genomic Scans.
P. Pavlidis, J. D. Jensen, W. Stephan, and A. Stamatakis (2012)
Mol. Biol. Evol. 29, 3237-3248
   Abstract »    Full Text »    PDF »
The Ability to Entrain to Long Photoperiods Differs between 3 Drosophila melanogaster Wild-Type Strains and Is Modified by Twilight Simulation.
D. Rieger, N. Peschel, V. Dusik, S. Glotz, and C. Helfrich-Forster (2012)
J Biol Rhythms 27, 37-47
   Abstract »    Full Text »    PDF »
Developmental trajectories of gene expression reveal candidates for diapause termination: a key life-history transition in the apple maggot fly Rhagoletis pomonella.
G. J. Ragland, S. P. Egan, J. L. Feder, S. H. Berlocher, and D. A. Hahn (2011)
J. Exp. Biol. 214, 3948-3960
   Abstract »    Full Text »    PDF »
Genomic Differentiation Between Temperate and Tropical Australian Populations of Drosophila melanogaster.
B. Kolaczkowski, A. D. Kern, A. K. Holloway, and D. J. Begun (2011)
Genetics 187, 245-260
   Abstract »    Full Text »    PDF »
Toward a synthetic understanding of the role of phenology in ecology and evolution.
J. Forrest and A. J. Miller-Rushing (2010)
Phil Trans R Soc B 365, 3101-3112
   Abstract »    Full Text »    PDF »
What Season Is It Anyway? Circadian Tracking vs. Photoperiodic Anticipation in Insects.
W. E. Bradshaw and C. M. Holzapfel (2010)
J Biol Rhythms 25, 155-165
   Abstract »    PDF »
The Clock Gene period Plays an Essential Role in Photoperiodic Control of Nymphal Development in the Cricket Modicogryllus siamensis.
T. Sakamoto, O. Uryu, and K. Tomioka (2009)
J Biol Rhythms 24, 379-390
   Abstract »    PDF »
Roles of PER immunoreactive neurons in circadian rhythms and photoperiodism in the blow fly, Protophormia terraenovae.
S. Shiga and H. Numata (2009)
J. Exp. Biol. 212, 867-877
   Abstract »    Full Text »    PDF »
Mendelian Inheritance of Pupal Diapause in the Flesh Fly, Sarcophaga bullata.
B. Han and D. L. Denlinger (2009)
J. Hered. 100, 251-255
   Abstract »    Full Text »    PDF »
A latitudinal cline in the Chinook salmon (Oncorhynchus tshawytscha) Clock gene: evidence for selection on PolyQ length variants.
K. G O'Malley and M. A Banks (2008)
Proc R Soc B 275, 2813-2821
   Abstract »    Full Text »    PDF »
An amino acid polymorphism in the couch potato gene forms the basis for climatic adaptation in Drosophila melanogaster.
P. S. Schmidt, C.-T. Zhu, J. Das, M. Batavia, L. Yang, and W. F. Eanes (2008)
PNAS 105, 16207-16211
   Abstract »    Full Text »    PDF »
TIMELESS Is an Important Mediator of CK2 Effects on Circadian Clock Function In Vivo.
R.-A. Meissner, V. L. Kilman, J.-M. Lin, and R. Allada (2008)
J. Neurosci. 28, 9732-9740
   Abstract »    Full Text »    PDF »
Genetic Differences in Human Circadian Clock Genes among Worldwide Populations.
C. M. Ciarleglio, K. K. Ryckman, S. V. Servick, A. Hida, S. Robbins, N. Wells, J. Hicks, S. A. Larson, J. P. Wiedermann, K. Carver, et al. (2008)
J Biol Rhythms 23, 330-340
   Abstract »    PDF »
Photoperiodic Induction of Diapause Requires Regulated Transcription of timeless in the Larval Brain of Chymomyza costata.
J. Stehlik, R. Zavodska, K. Shimada, I. Sauman, and V. Kostal (2008)
J Biol Rhythms 23, 129-139
   Abstract »    PDF »
TIMELESS CLOCK.
H. Merzendorfer (2007)
J. Exp. Biol. 210, vii
   Full Text »    PDF »
Rhythm Defects Caused by Newly Engineered Null Mutations in Drosophila's cryptochrome Gene.
E. Dolezelova, D. Dolezel, and J. C. Hall (2007)
Genetics 177, 329-345
   Abstract »    Full Text »    PDF »
EVOLUTION: Tantalizing timeless.
W. Bradshaw and C. Holzapfel (2007)
Science 316, 1851-1852
   Abstract »    Full Text »    PDF »
A Molecular Basis for Natural Selection at the timeless Locus in Drosophila melanogaster.
F. Sandrelli, E. Tauber, M. Pegoraro, G. Mazzotta, P. Cisotto, J. Landskron, R. Stanewsky, A. Piccin, E. Rosato, M. Zordan, et al. (2007)
Science 316, 1898-1900
   Abstract »    Full Text »    PDF »
Principles and Problems Revolving Round Rhythm-related Genetic Variants.
J. C. Hall, D. C. Chang, and E. Dolezelova (2007)
Cold Spring Harb Symp Quant Biol 72, 215-232
   Abstract »    PDF »
Thermosensitive Splicing of a Clock Gene and Seasonal Adaptation.
W.-F. Chen, K. H. Low, C. Lim, and I. Edery (2007)
Cold Spring Harb Symp Quant Biol 72, 599-606
   Abstract »    PDF »

To Advertise     Find Products


Science Signaling. ISSN 1937-9145 (online), 1945-0877 (print). Pre-2008: Science's STKE. ISSN 1525-8882