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.

Science 19 December 1997:
Vol. 278. no. 5346, pp. 2117 - 2120
DOI: 10.1126/science.278.5346.2117
Prev | Table of Contents | Next

Reports

Natural Variation in a Drosophila Clock Gene and Temperature Compensation

Lesley A. Sawyer, * J. Michael Hennessy, * Alexandre A. Peixoto, dagger Ezio Rosato, Helen Parkinson, Rodolfo Costa, Charalambos P. Kyriacou ddagger

The threonine-glycine (Thr-Gly) encoding repeat within the clock gene period of Drosophila melanogaster is polymorphic in length. The two major variants (Thr-Gly)17 and (Thr-Gly)20 are distributed as a highly significant latitudinal cline in Europe and North Africa. Thr-Gly length variation from both wild-caught and transgenic individuals is related to the flies' ability to maintain a circadian period at different temperatures. This phenomenon provides a selective explanation for the geographical distribution of Thr-Gly lengths and gives a rare glimpse of the interplay between molecular polymorphism, behavior, population biology, and natural selection.

L. A. Sawyer, J. M. Hennessy, A. A. Peixoto, E. Rosato, H. Parkinson, C. P. Kyriacou, Department of Genetics, University of Leicester, LE1 7RH, UK.
R. Costa, Dipartimento di Biologia, Universitá di Padova, Via Trieste 75, 35121 Padova, Italy.
*   These authors contributed equally to this work.

dagger    Present address: Departamento de Bioquimica e Biologia Molecular Fundacao Oswaldo Cruz, Avenue Brasil, 4365-Manquinhos, CEP 21045-900, Rio de Janeiro, Brazil.

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

Read the Full Text


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Synergic Entrainment of Drosophila's Circadian Clock by Light and Temperature.
T. Yoshii, S. Vanin, R. Costa, and C. Helfrich-Forster (2009)
J Biol Rhythms 24, 452-464
   Abstract »    PDF »
Global Microsatellite Content Distinguishes Humans, Primates, Animals, and Plants.
C.L. Galindo, L.J. McIver, J.F. McCormick, M.A. Skinner, Y. Xie, R.A. Gelhausen, K. Ng, N.M. Kumar, and H.R. Garner (2009)
Mol. Biol. Evol. 26, 2809-2819
   Abstract »    Full Text »    PDF »
CKI{varepsilon}/{delta}-dependent phosphorylation is a temperature-insensitive, period-determining process in the mammalian circadian clock.
Y. Isojima, M. Nakajima, H. Ukai, H. Fujishima, R. G. Yamada, K.-h. Masumoto, R. Kiuchi, M. Ishida, M. Ukai-Tadenuma, Y. Minami, et al. (2009)
PNAS 106, 15744-15749
   Abstract »    Full Text »    PDF »
Comparative and Functional Characterization of Intragenic Tandem Repeats in 10 Aspergillus Genomes.
J. G. Gibbons and A. Rokas (2009)
Mol. Biol. Evol. 26, 591-602
   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 »
Genomic Analysis of Adaptive Differentiation in Drosophila melanogaster.
T. L. Turner, M. T. Levine, M. L. Eckert, and D. J. Begun (2008)
Genetics 179, 455-473
   Abstract »    Full Text »    PDF »
Avian circannual clocks: adaptive significance and possible involvement of energy turnover in their proximate control.
M. Wikelski, L. B Martin, A. Scheuerlein, M. T Robinson, N. D Robinson, B. Helm, M. Hau, and E. Gwinner (2008)
Phil Trans R Soc B 363, 411-423
   Abstract »    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 »
Natural Selection Favors a Newly Derived timeless Allele in Drosophila melanogaster.
E. Tauber, M. Zordan, F. Sandrelli, M. Pegoraro, N. Osterwalder, C. Breda, A. Daga, A. Selmin, K. Monger, C. Benna, et al. (2007)
Science 316, 1895-1898
   Abstract »    Full Text »    PDF »
Synchronization of the Drosophila Circadian Clock by Temperature Cycles.
F. T. Glaser and R. Stanewsky (2007)
Cold Spring Harb Symp Quant Biol 72, 233-242
   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 »
Drosophila flies in "Evolution Canyon" as a model for incipient sympatric speciation.
A. Korol, E. Rashkovetsky, K. Iliadi, and E. Nevo (2006)
PNAS 103, 18184-18189
   Abstract »    Full Text »    PDF »
Diversity of zebrafish peripheral oscillators revealed by luciferase reporting.
M. Kaneko, N. Hernandez-Borsetti, and G. M. Cahill (2006)
PNAS 103, 14614-14619
   Abstract »    Full Text »    PDF »
The period Gene Thr-Gly Polymorphism in Australian and African Drosophila melanogaster Populations: Implications for Selection.
L. A. Sawyer, F. Sandrelli, C. Pasetto, A. A. Peixoto, E. Rosato, R. Costa, and C. P. Kyriacou (2006)
Genetics 174, 465-480
   Abstract »    Full Text »    PDF »
Histamine and its receptors modulate temperature-preference behaviors in Drosophila..
S.-T. Hong, S. Bang, D. Paik, J. Kang, S. Hwang, K. Jeon, B. Chun, S. Hyun, Y. Lee, and J. Kim (2006)
J. Neurosci. 26, 7245-7256
   Abstract »    Full Text »    PDF »
The Molecular Basis of Temperature Compensation in the Arabidopsis Circadian Clock.
P. D. Gould, J. C.W. Locke, C. Larue, M. M. Southern, S. J. Davis, S. Hanano, R. Moyle, R. Milich, J. Putterill, A. J. Millar, et al. (2006)
PLANT CELL 18, 1177-1187
   Abstract »    Full Text »    PDF »
Plant circadian rhythms..
C. R. McClung (2006)
PLANT CELL 18, 792-803
   Full Text »    PDF »
Analysis of Phase of LUCIFERASE Expression Reveals Novel Circadian Quantitative Trait Loci in Arabidopsis.
C. Darrah, B. L. Taylor, K. D. Edwards, P. E. Brown, A. Hall, and H. G. McWatters (2006)
Plant Physiology 140, 1464-1474
   Abstract »    Full Text »    PDF »
FLOWERING LOCUS C Mediates Natural Variation in the High-Temperature Response of the Arabidopsis Circadian Clock.
K. D. Edwards, P. E. Anderson, A. Hall, N. S. Salathia, J. C.W. Locke, J. R. Lynn, M. Straume, J. Q. Smith, and A. J. Millar (2006)
PLANT CELL 18, 639-650
   Abstract »    Full Text »    PDF »
Independence of Genetic Geographical Variation between Photoperiodic Diapause, Circadian Eclosion Rhythm, and Thr-Gly Repeat Region of the Period Gene in Drosophila littoralis.
P. Lankinen and P. Forsman (2006)
J Biol Rhythms 21, 3-12
   Abstract »    PDF »
Evolution of a Length Polymorphism in the Human PER3 Gene, a Component of the Circadian System.
N. A. Nadkarni, M. E. Weale, M. von Schantz, and M. G. Thomas (2005)
J Biol Rhythms 20, 490-499
   Abstract »    PDF »
Natural Allelic Variation in the Temperature-Compensation Mechanisms of the Arabidopsis thaliana Circadian Clock.
K. D. Edwards, J. R. Lynn, P. Gyula, F. Nagy, and A. J. Millar (2005)
Genetics 170, 387-400
   Abstract »    Full Text »    PDF »
Enhanced Fitness Conferred by Naturally Occurring Variation in the Circadian Clock.
T. P. Michael, P. A. Salome, H. J. Yu, T. R. Spencer, E. L. Sharp, M. A. McPeek, J. M. Alonso, J. R. Ecker, and C. R. McClung (2003)
Science 302, 1049-1053
   Abstract »    Full Text »    PDF »
Genetic Differentiation Between American and European Drosophila melanogaster Populations Could Be Attributed to Admixture of African Alleles.
G. Caracristi and C. Schlotterer (2003)
Mol. Biol. Evol. 20, 792-799
   Abstract »    Full Text »    PDF »
Origins of Circadian Rhythmicity.
E. Rosato and C. P. Kyriacou (2002)
J Biol Rhythms 17, 506-511
   PDF »
Insect Photoperiodism and Circadian Clocks: Models and Mechanisms.
E. Tauber and B. P. Kyriacou (2001)
J Biol Rhythms 16, 381-390
   Abstract »    PDF »
Seasonality and Photoperiodism in Fungi.
T. Roenneberg and M. Merrow (2001)
J Biol Rhythms 16, 403-414
   Abstract »    PDF »
Squaring Up the E-box.
C. P. Kyriacou and E. Rosato (2000)
J Biol Rhythms 15, 483-490
   PDF »
Altered Entrainment and Feedback Loop Function Effected by a Mutant Period Protein.
P. Schotland, M. Hunter-Ensor, T. Lawrence, and A. Sehgal (2000)
J. Neurosci. 20, 958-968
   Abstract »    Full Text »    PDF »
The Clock Gene period of the Housefly, Musca domestica, Rescues Behavioral Rhythmicity in Drosophila melanogaster: Evidence for Intermolecular Coevolution?.
A. Piccin, M. Couchman, J. D. Clayton, D. Chalmers, R. Costa, and C. P. Kyriacou (2000)
Genetics 154, 747-758
   Abstract »    Full Text »
timrit Lengthens Circadian Period in a Temperature-Dependent Manner through Suppression of PERIOD Protein Cycling and Nuclear Localization.
A. Matsumoto, K. Tomioka, Y. Chiba, and T. Tanimura (1999)
Mol. Cell. Biol. 19, 4343-4354
   Abstract »    Full Text »    PDF »
Effects of Circadian Mutations and LD Periodicity on the Life Span of Drosophila melanogaster.
A. Klarsfeld and F. Rouyer (1998)
J Biol Rhythms 13, 471-478
   Abstract »    PDF »
Synaptic inhibition: its role in suprachiasmatic nucleus neuronal thermosensitivity and temperature compensation in the rat.
P W Burgoon and J A Boulant (1998)
J. Physiol. 512, 793-807
   Abstract »    Full Text »    PDF »
The timSL Mutant Affects a Restricted Portion of the Drosophila melanogaster Circadian Cycle.
J. E. Rutila, O. Maltseva, and M. Rosbash (1998)
J Biol Rhythms 13, 380-392
   Abstract »    PDF »
Short-Sequence DNA Repeats in Prokaryotic Genomes.
A. van Belkum, S. Scherer, L. van Alphen, and H. Verbrugh (1998)
Microbiol. Mol. Biol. Rev. 62, 275-293
   Abstract »    Full Text »    PDF »
Molecular and Behavioral Analysis of Four period Mutants in Drosophila melanogaster Encompassing Extreme Short, Novel Long, and Unorthodox Arrhythmic Types.
M. J. Hamblen, N. E. White, P. T. J. Emery, K. Kaiser, and J. C. Hall (1998)
Genetics 149, 165-178
   Abstract »    Full Text »    PDF »
Molecular coevolution within a Drosophila clock gene.
A. A. Peixoto, J. M. Hennessy, I. Townson, G. Hasan, M. Rosbash, R. Costa, and C. P. Kyriacou (1998)
PNAS 95, 4475-4480
   Abstract »    Full Text »    PDF »
Neuronal Polymorphism among Natural Alleles of a cGMP-Dependent Kinase Gene, foraging, in Drosophila.
J. J. Renger, W.-D. Yao, M. B. Sokolowski, and C.-F. Wu (1999)
J. Neurosci. 19, RC28
   Abstract »    Full Text »    PDF »


To Advertise     Find Products

Science. ISSN 0036-8075 (print), 1095-9203 (online)