Cited by 308Circadian rhythm and melatoninEvolution and Genetic DynamicsPhysiological and biochemical adaptations

The DOI matches its Crossref record; 23 of the 23 references it cites were found in a registry or an index.

Natural Selection Favors a Newly Derived timeless Allele in Drosophila melanogaster

Tauber, Eran, Zordan, Mauro, Sandrelli, Federica, Pegoraro, Mirko, Osterwalder, Nicolò, Breda, Carlo, Daga, Andrea, Selmin, Alessandro, Monger, Karen, Benna, Clara, Rosato, Ezio, Kyriacou, Charalambos P., Costa, Rodolfo·2007·Science

DOI 10.1126/science.1138412

Open this paper in CoChat — free account

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.

Integrity signals

Registry

Crossref · 10.1126/science.1138412

Cites

23 of 23 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Statistical method for testing the neutral mutation hypothesis by DNA polymorphism.
Tajima, F. (1989) · Genetics · doi:10.1093/genetics/123.3.585 · Cited by 14,056
Statistical tests of neutrality of mutations.
Fu, Y., & Li, W. (1993) · Genetics · doi:10.1093/genetics/133.3.693 · Cited by 4,051
A Test of Neutral Molecular Evolution Based on Nucleotide Data
Hudson, R. R., Kreitman, M., & Aguadé, M. (1987) · Genetics · doi:10.1093/genetics/116.1.153 · Cited by 1,759
A Single Amino Acid Mutation Contributes to Adaptive Beach Mouse Color Pattern
Hoekstra, H. E., Hirschmann, R. J., Bundey, R. A., Insel, P. A., & Crossland, J. P. (2006) · Science · doi:10.1126/science.1126121 · Cited by 716
Historical Biogeography of the Drosophila melanogaster Species Subgroup
Lachaise, D., Cariou, M. L., David, J. R., Lemeunier, F., Tsacas, L., & Ashburner, M. (1988) · Springer eBooks · doi:10.1007/978-1-4613-0931-4_4 · Cited by 624
Molecular phylogeny and divergence times of drosophilid species.
Russo, C., Takezaki, N., & Nei, M. (1995) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a040214 · Cited by 578
Natural Variation in a Drosophila Clock Gene and Temperature Compensation
Sawyer, L., Hennessy, J. M., Peixoto, A. A., Rosato, E., Parkinson, H., Costa, R., & Kyriacou, C. P. (1997) · Science · doi:10.1126/science.278.5346.2117 · Cited by 320
Induction of diapause in Drosophila melanogaster: photoperiodic regulation and the impact of arrhythmic clock mutations on time measurement.
Saunders, D. S., Henrich, V. C., & Gilbert, L. I. (1989) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.86.10.3748 · Cited by 306
GEOGRAPHIC VARIATION IN DIAPAUSE INCIDENCE, LIFE‐HISTORY TRAITS, AND CLIMATIC ADAPTATION INDROSOPHILA MELANOGASTER
SCHMIDT, P. S., Matzkin, L. M., Ippolito, M., & Eanes, W. F. (2005) · Evolution · doi:10.1111/j.0014-3820.2005.tb01821.x · Cited by 290
Evidence for positive selection in the superoxide dismutase (Sod) region of Drosophila melanogaster.
Hudson, R. R., Bailey, K., Skarecky, D. W., Kwiatowski, J., & Ayala, F. J. (1994) · Genetics · doi:10.1093/genetics/136.4.1329 · Cited by 276

Flagged first, then by citations

Show all 23 references

Research works printed but not linked: 3

C. A. Russo, N. Takezaki, M. Nei, Mol. Biol. Evol.12, 391 (1995).
D. Lachaiseet al., Evol. Biol.22, 159 (1988).
P. S. Schmidt, L. Matzkin, M. Ippollito, W. Eanes, Evolution59, 1721 (2005).

Sorted by citations

Items 201–300 of 308

Comparative Transcriptome Analysis Reveals bmo-miR-6497-3p Regulate Circadian Clock Genes during the Embryonic Diapause Induction Process in Bivoltine Silkworm
Liu, L., Zhang, P., Gao, Q., Feng, X., Han, L., Zhang, F., Bai, Y., Han, M., Hu, H., Dai, F., et al. (2021) · Insects · doi:10.3390/insects12080739 · Cited by 11
“In Drosophila melanogaster, lack of the timeless gene leads to a reduction in diapause rates [15].”
Background
Geography of the circadian gene clock and photoperiodic response in western North American populations of the three‐spined sticklebackGasterosteus aculeatus
O'Brien, C., Unruh, L., Zimmerman, C. E., Bradshaw, W. E., Holzapfel, C. M., & Cresko, W. A. (2013) · Journal of Fish Biology · doi:10.1111/jfb.12024 · Cited by 11
Lack of association between winter coat colour and genetic population structure in the Japanese hare,Lepus brachyurus(Lagomorpha: Leporidae)
Nunome, M., Kinoshita, G., Tomozawa, M., Torii, H., Matsuki, R., Yamada, F., Matsuda, Y., & Suzuki, H. (2014) · Biological Journal of the Linnean Society · doi:10.1111/bij.12245 · Cited by 11
Molecular Evolution of a Pervasive Natural Amino-Acid Substitution in Drosophila cryptochrome
Pegoraro, M., Noreen, S., Bhavnani, S., Tsolou, A., Schmid, R., Kyriacou, C. P., & Tauber, E. (2014) · PLoS ONE · doi:10.1371/journal.pone.0086483 · Cited by 11
“The tim variants’ differential light responses in both their circadian behaviour and photoperiodic diapause mechanisms suggest a possible seasonal adaptation that may drive the positive selection of the new variant in the temperate European environment [8,9].”
BackgroundInfluential
Robustness of Circadian Timing Systems Evolves in the Fruit FlyDrosophila melanogasteras a Correlated Response to Selection for Adult Emergence in a Narrow Window of Time
Kannan, N. N., Mukherjee, N., & Sharma, V. K. (2012) · Chronobiology International · doi:10.3109/07420528.2012.728550 · Cited by 11
“, 1997), and tim polymorphism is thought to be involved in the seasonal adaptation of circadian rhythms (Kyriacou et al., 2008; Tauber et al., 2007).”
Background
Genomic signals of local adaptation across climatically heterogenous habitats in an invasive tropical fruit fly (Bactrocera tryoni)
Parvizi, E., Vaughan, A. L., Dhami, M. K., & McGaughran, A. (2023) · Heredity · doi:10.1038/s41437-023-00657-y · Cited by 10
“Candidate genes, such as protein timeless and hormone receptor 4, have been implicated in diapause regulation (e.g., in Drosophila , Tauber et al. 2007) and mating receptivity in insects (Ma et al. 2021).”
Background
Evolution: How Fruit Flies Adapt to Seasonal Stresses
Williams, K. D., & Sokolowski, M. B. (2009) · Current Biology · doi:10.1016/j.cub.2008.11.035 · Cited by 10
Life-history traits of Drosophila melanogaster populations exhibiting early and late eclosion chronotypes
Nikhil, K. L., Ratna, K., & Sharma, V. K. (2016) · BMC Evolutionary Biology · doi:10.1186/s12862-016-0622-3 · Cited by 10
“In addition, studies on organisms inhabiting different latitudes, as well as those living in constant conditions reported large variation in circadian phenotypes in accordance to their local habitats, suggesting that the underlying clocks may have evolved as an adaptation to the presence or absence of cyclic environme…”
Background
Genomic Responses to Climate Change: Making the Most of the Drosophila Model
Rodrigues, M. F., & Cogni, R. (2021) · Frontiers in Genetics · doi:10.3389/fgene.2021.676218 · Cited by 9
“melanogaster is nonetheless a great system to dissect the genetic bases of adaptation in detail (Tauber et al., 2007; Schmidt et al., 2008; Erickson et al., 2020).”
Background
Molecular Mechanisms of Photoperiodism
Goto, S. G. (2023) · Entomology monographs · doi:10.1007/978-981-99-0726-7_13 · Cited by 9
2mit, an Intronic Gene of Drosophila melanogaster timeless2, Is Involved in Behavioral Plasticity
Baggio, F., Bozzato, A., Benna, C., Leonardi, E., Romoli, O., Cognolato, M., Tosatto, S. C. E., Costa, R., & Sandrelli, F. (2013) · PLoS ONE · doi:10.1371/journal.pone.0076351 · Cited by 9
“significantly influences circadian light responses [23,24], we”
Method
In silico analyses of CD14 molecule reveal significant evolutionary diversity, potentially associated with speciation and variable immune response in mammals
Morenikeji, O. B., & Thomas, B. N. (2019) · PeerJ · doi:10.7717/peerj.7325 · Cited by 10
“In addition, this reveals the common origin between the mammalian species before divergent speciation (Tauber et al., 2007).”
Background
Natural selection on sleep duration in Drosophila melanogaster
Souto-Maior, C., Negron, Y. L. S., & Harbison, S. T. (2020) · Scientific Reports · doi:10.1038/s41598-020-77680-0 · Cited by 9
Clock-talk: have we forgotten about geographic variation?
Bradshaw, W. E., Fletcher, M. C., & Holzapfel, C. M. (2023) · Journal of Comparative Physiology A · doi:10.1007/s00359-023-01643-9 · Cited by 9
“…is the s-tim and ls-tim polymorphism that affects clock performance, and pleiotropically, the incidence of diapause (Tauber et al. 2007; Sandrelli et al. 2007), development time, and early fecundity (Andreatta et al. 2023), but not photoperiod x clock genotype interaction (Tauber et al. 2007, Fig.”
Background
Photoperiodism in Insects: Molecular Basis and Consequences of Diapause
Williams, K. D., SCHMIDT, P. S., & Sokolowski, M. B. (2009) · doi:10.1093/acprof:oso/9780195335903.003.0012 · Cited by 9
Knockdown of timeless Disrupts the Circadian Behavioral Rhythms in Laodelphax striatellus (Hemiptera: Delphacidae)
Jiang, Y.-D., Yuan, X., Bai, Y., Wang, G., Zhou, W., & Zhu, Z. (2018) · Environmental Entomology · doi:10.1093/ee/nvy095 · Cited by 9
Photosensitive Alternative Splicing of the Circadian Clock Gene timeless Is Population Specific in a Cold-Adapted Fly, Drosophila montana
Tapanainen, R., Parker, D. J., & Kankare, M. (2018) · G3 Genes Genomes Genetics · doi:10.1534/g3.118.200050 · Cited by 8
“…et al. 2007). s-tim appears to be the ancestral variant present in northern Europe, while ls-tim is a newer variant that has spread through Europe (Tauber et al. 2007). ls-tim makes the circadian clock in D. melanogaster less light-sensitive, which is thought to be favorable in colder climates…”
BackgroundInfluential
Biological Clocks and Rhythms in Polar Organisms
Last, K. S., Häfker, N. S., Hendrick, V. J., Meyer, B., Tran, D., & Piccolin, F. (2020) · Advances in polar ecology · doi:10.1007/978-3-030-33208-2_8 · Cited by 8
Comparative analysis of the circadian rhythm genes period and timeless in Culex pipiens Linnaeus, 1758 (Diptera, Culicidae)
Шайкевич, Е. В., Zakharov, I. S., & Fyodorova, M. V. (2016) · Comparative Cytogenetics · doi:10.3897/compcytogen.v10i4.7582 · Cited by 7
“Well-documented data have been reported showing that new native mutations sometimes are rapidly spreading in a population and that polymorphism in one locus may provide adaptive variations in behavioral and morphological phenotypes of the insects in nature (Tauber et al. 2007).”
Background
Interspecific studies of circadian genes period and timeless in Drosophila
Noreen, S., Pegoraro, M., Nouroz, F., Tauber, E., & Kyriacou, C. P. (2018) · Gene · doi:10.1016/j.gene.2018.01.020 · Cited by 7
“, 1996) and associated photoperiodic phenotypes such as diapause (Tauber et al., 2007).”
Background
Photoperiodism in Mollusks
Numata, H., & Udaka, H. (2009) · doi:10.1093/acprof:oso/9780195335903.003.0008 · Cited by 7
Effects of Food and Temperature on Drosophila melanogaster Reproductive Dormancy as Revealed by Quantification of a GFP-Tagged Yolk Protein in the Ovary
Hara, Y., & Yamamoto, D. (2022) · Frontiers in Physiology · doi:10.3389/fphys.2021.803144 · Cited by 6
Norpa Signalling and the Seasonal Circadian Locomotor Phenotype in Drosophila
Breda, C., Rosato, E., & Kyriacou, C. P. (2020) · Biology · doi:10.3390/biology9060130 · Cited by 6
Evolution of robust circadian clocks in Drosophila melanogaster populations reared in constant dark for over 330 generations
Shindey, R., Varma, V., Nikhil, K. L., & Sharma, V. K. (2016) · Die Naturwissenschaften · doi:10.1007/s00114-016-1399-3 · Cited by 6
Biological Timekeeping: Individual Variation, Performance, and Fitness
MacDougall‐Shackleton, S. A., Watts, H. E., & Hahn, T. P. (2014) · Integrative Organismal Biology · doi:10.1002/9781118398814.ch15 · Cited by 6
Continent-wide differentiation of fitness traits and patterns of climate adaptation among European populations of Drosophila melanogaster
Mitchell, E. D., Kerdaffrec, E., Harney, E., Paulo, T. F., Veselinović, M. S., Tanasković, M., Tyukmaeva, V. I., Abaurrea, T. M., Aksoy, C. F., Argyridou, E., et al. (2025) · Evolution Letters · doi:10.1093/evlett/qraf014 · Cited by 7
Neuropeptide dynamics coordinate layered plasticity mechanisms adapting Drosophila circadian behavior to changing environment
Chatterjee, A., De, J., Martin, B., Chélot, E., Zhong, P., & Rouyer, F. (2025) · Science Advances · doi:10.1126/sciadv.adt7168 · Cited by 5
Mapping Quantitative Trait Loci Underlying Circadian Light Sensitivity in Drosophila
Adewoye, A., Nuzhdin, S., & Tauber, E. (2017) · bioRxiv · doi:10.1177/0748730417731863 · Cited by 4
“Later, a natural polymorphism in the light-sensitive clock protein TIM was identified in D. melanogaster (Tauber et al. 2007).”
BackgroundResultInfluential
Nucleotide Variation in Drosophila cryptochrome Is Linked to Circadian Clock Function: An Association Analysis
Pegoraro, M., Rezek, E. S., Fishman, B., & Tauber, E. (2022) · Frontiers in Physiology · doi:10.3389/fphys.2022.781380 · Cited by 5
RNA-seq analysis to identify genes related to resting egg production of panarctic Daphnia pulex
Maruoka, N., Makino, T. T., & Urabe, J. (2023) · BMC Genomics · doi:10.1186/s12864-023-09369-3 · Cited by 5
Extreme Conservation and Non-Neutral Evolution of the cpmA Circadian Locus in a Globally Distributed Chroococcidiopsis sp. from Naturally Stressful Habitats
Dvornyk, V., & Jahan, A. S. (2012) · Molecular Biology and Evolution · doi:10.1093/molbev/mss191 · Cited by 5
“Natural selection was also reported to operate on another Drosophila circadian gene, timeless (Tauber et al. 2007).”
Background
Interpreting Seasonal Cues to Program Diapause Entry
Denlinger, D. L. (2022) · Cambridge University Press eBooks · doi:10.1017/9781108609364.006 · Cited by 4
Molecular Signaling Pathways that Regulate Diapause
Denlinger, D. L. (2022) · Cambridge University Press eBooks · doi:10.1017/9781108609364.010 · Cited by 5
Natural alleles of the clock gene timeless differentially affect life-history traits in Drosophila
Andreatta, G., Montagnese, S., & Costa, R. (2023) · Frontiers in Physiology · doi:10.3389/fphys.2022.1092951 · Cited by 5
“For instance, the different propensity to undergo dormancy of homozygous flies for one of the two variants (s-tim and ls-tim) (Tauber et al., 2007) has been linked to the different affinity of S-TIM and L-TIM for CRY, the blue-light photoreceptor, which mediates TIM light-dependent degradation and, in turn, clock rese…”
BackgroundMethodInfluential
Clock Gene Evolution: Seasonal Timing, Phylogenetic Signal, or Functional Constraint?
Krabbenhoft, T. J., & Turner, T. F. (2014) · Journal of Heredity · doi:10.1093/jhered/esu008 · Cited by 5
“In the Rio Grande in New Mexico, USA, members of the fish community exhibit partially overlapping, but distinct, spawning seasons (Turner et al. 2010; Krabbenhoft TJ et al., unpublished data).”
BackgroundMethod
Principles and Problems Revolving Round Rhythm-related Genetic VariantsPreprint
Hall, J. C., Chang, D. C., & Doleželová, E. (2007) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.2007.72.039 · Cited by 5
Dissecting the Interaction between Cryptochrome and Timeless Reveals Underpinnings of Light-Dependent Recognition
Schneps, C. M., Dunleavy, R., & Crane, B. R. (2024) · Biochemistry · doi:10.1021/acs.biochem.3c00630 · Cited by 4
Evolution: Fruit Fly Clocks on the Edge
Kyriacou, C. P. (2017) · Current Biology · doi:10.1016/j.cub.2017.02.017 · Cited by 4
“While it is not clear how differences in seasonal locomotor behaviour profiles might adapt different species to the latitudes, perhaps there is a more fundamental aspect of seasonal physiology/behaviour that is also being affected? The ls-tim variant has an additional phenotype, a higher propensity to overwinter or di…”
BackgroundInfluential
Partial reuse of circadian clock genes along parallel clines of diapause in two moth species
Yu, Y., Huang, L., Xue, F., & Dopman, E. B. (2023) · Molecular Ecology · doi:10.1111/mec.16940 · Cited by 4
Environmental Adaptation and Evolution of Circadian Clocks
Dani, C., Kannan, N. N., & Sheeba, V. (2023) · Entomology monographs · doi:10.1007/978-981-99-0726-7_9 · Cited by 3
The Diapause State
Denlinger, D. L. (2022) · Cambridge University Press eBooks · doi:10.1017/9781108609364.008 · Cited by 3
Unveiling Subtle Geographical Clines: Phenotypic Effects and Dynamics of Circadian Clock Gene Polymorphisms
Khatib, L., Subasi, B. S., Fishman, B., Kapun, M., & Tauber, E. (2023) · Biology · doi:10.3390/biology12060858 · Cited by 3
“A latitude cline was also found in tim [9].”
Background
Testing for variation in photoperiodic plasticity in a butterfly: Inconsistent effects of circadian genes between geographic scales
Lindestad, O., Nylin, S., Wheat, C. W., & Gotthard, K. (2024) · Ecology and Evolution · doi:10.1002/ece3.11713 · Cited by 3
Circadian clock genes and seasonal behaviour
Gesto, J. S. M. (2011) · Figshare · Cited by 3
Seasonal variation in endoreduplication and polyteny in the fruit fly Drosophila melanogaster (Diptera: Drosophilidae): How does it contribute to adaptation?
Strashnyuk, V., Vakulenko, E., & Koptevtsova, Y. (2025) · European Journal of Entomology · doi:10.14411/eje.2025.001 · Cited by 2
Cold-Sensing TRP Channels and Temperature Preference Modulate Ovarian Development in the Model Organism Drosophila melanogaster
Andreatta, G., Montagnese, S., & Costa, R. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26125638 · Cited by 2
“Briefly, genomic DNA was extracted from 5–10 females from each strain and amplified using Amplification Refractory Mutation System (ARMS) PCR [74] with the following primers: ls-tim forward: 5 ′ -TGGAATAATCAGAACTTTGA-3 ′ ; s-tim forward: 5 ′ -TGGAATAATCAGAACTTTAT-3 ′ ; s-tim reverse: 5 ′…”
Influential
No lazing on sunny afternoons
Rouyer, F. (2012) · Nature · doi:10.1038/484325a · Cited by 2
Divergence in cell cycle progression is associated with shifted phenology in a multivoltine moth: the European corn borer, Ostrinia nubilalis
Xia, Q., Chen, C., Dopman, E. B., & Hahn, D. A. (2023) · Journal of Experimental Biology · doi:10.1242/jeb.245244 · Cited by 2
Plausible neural circuitry for photoperiodism in the blow fly,Protophormia terraenovae
Shiga, S. (2012) · Acta Biologica Hungarica · doi:10.1556/abiol.63.2012.suppl.2.3 · Cited by 2
“later, it has been suggested that timeless directly affects incidence of diapause through circadian photoreception [21, 29].”
Background
Preparing for Diapause
Denlinger, D. L. (2022) · Cambridge University Press eBooks · doi:10.1017/9781108609364.007 · Cited by 2
Confronting the Challenges of a Seasonal Environment
Denlinger, D. L. (2022) · Cambridge University Press eBooks · doi:10.1017/9781108609364.002 · Cited by 3
OVERVIEW
Denlinger, D. L. (2009) · doi:10.1093/acprof:oso/9780195335903.003.0024 · Cited by 2
Editorial: Biological rhythms: Evolution, population biology, and adaptation
Kyriacou, C. P., Menegazzi, P., & Doležel, D. (2023) · Frontiers in Physiology · doi:10.3389/fphys.2023.1157631 · Cited by 2
“In this context, within our Research Topic, Andreatta et al. explore the life-history implications of the two Drosophila tim alleles mentioned earlier. ls-tim circadian photoresponses and diapause favour it in any seasonal environment (such as Europe) so eventually, this novel beneficial mutation may eliminate s-tim.”
BackgroundInfluential
The period gene alters daily and seasonal timing in Ostrinia nubilalisPreprint
Dayton, J. N., & Dopman, E. B. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.11.02.621642 · Cited by 2
“Geographic variation in diapause timing has frequently been associated with both allelic variation in clock genes 13–18 and differences in circadian timing 19–21 .”
Background
Which Seasons Are Being Avoided?
Denlinger, D. L. (2022) · Cambridge University Press eBooks · doi:10.1017/9781108609364.003 · Cited by 1
Insect circadian plasticity as a proposed target for the expression of parasite extended phenotypes
Dopp, J., & de Bekker, C. (2025) · npj Biological Timing and Sleep · doi:10.1038/s44323-025-00046-0 · Cited by 1
Timeless ‐ BmaaNAT axis regulates temperature‐dependent diapause plasticity in the silkworm, Bombyx mori
Liu, L., Yang, C., Zheng, L., Idris, N. F. B., Liu, Z., Yuan, Y., Song, J., Zhou, L., Dai, F., & Tong, X. (2025) · Insect Science · doi:10.1111/1744-7917.70218 · Cited by 1
Geographic Divergence and the Genomic Basis of Reproductive Diapause in Drosophila triauraria
Fujichika, T., Aoyama, Y., Onuma, M., Nozawa, M., & Takahashi, A. (2026) · Molecular Ecology · doi:10.1111/mec.70251 · Cited by 1
“L isoform ( ls-tim and s - tim ) are known to regulate diapause induction (Tauber et al. 2007; Sandrelli et al. 2007), and accumulation of TIM-SC under low temperature, short-day conditions is implicated in diapause regulation by stabilising Eyes absent (EYA) (Abrieux et al. 2020).”
Influential
The utility and use of solitary bees for pollination in greenhouses and other covered growing systems: A review
Hogendoorn, K., & Evans, L. J. (2026) · Current Research in Insect Science · doi:10.1016/j.cris.2026.100126 · Cited by 1
“Environmental influences may work indirectly via effects on the mother, or directly via effects on the development of the brood (Tepedino and Parker 1986; Tauber et al. 2007).”
Splicing of a core circadian clock gene regulates seasonal adaptations by a winter gating mechanism
Hidalgo, S., Rio, R. D., Tabuloc, C. A., Hernandez, L. A. P., Berry, A. L., Cai, Y. D., Lewald, K. M., & Chiu, J. C. (2026) · Science Advances · doi:10.1126/sciadv.aed4249 · Cited by 1
The Evolutionary Genetics of Life History in Drosophila Melanogaster
Paaby, A. B. (2009) · ScholarlyCommons (University of Pennsylvania) · Cited by 1
Genetic architecture underlying morning and evening circadian phenotypes in fruit flies Drosophila melanogaster
Vaze, K. M., Nikhil, K. L., & Sharma, V. K. (2013) · Heredity · doi:10.1038/hdy.2013.28 · Cited by 1
“Candidate gene studies based on genes identified through classical mutagenesis approach (Costa et al., 1992; Tauber et al., 2007), and quantitative trait locus analysis of circadian phenotypes (Michael et al., 2003; Kim et al., 2007), have helped in identifying the genetic basis of naturally…”
Background
Learning to collaborate: bringing together behavior and quantitative genomics
Williams‐Simon, P. A., Ganesan, M., & King, E. G. (2020) · Journal of Neurogenetics · doi:10.1080/01677063.2019.1710145 · Cited by 1
“…identify naturally occurring genetic variants influencing behaviors such as learning (Anreiter & Sokolowski, 2019; Mery, Belay, So, Sokolowski, & Kawecki, 2007) circadian rhythm (Tauber et al., 2007); (Bauzer, Souza, Ward, Kyriacou, & Peixoto, 2002), and pupation (Zhang, Guy Reeves, & Tautz, 2019).”
A latitudinal cline in a courtship song character of Drosophila melanogaster
Stanley, R. A., & Kyriacou, C. P. (2021) · Journal of Neurogenetics · doi:10.1080/01677063.2021.1933968 · Cited by 1
“Indeed one of her papers on geographical variation in diapause in Drosophila melanogaster (Williams & Sokolowski, 1993) stimulated me (CPK) to work on this seasonal phenotype (Sandrelli et al., 2007; Tauber et al., 2007).”
Background
Control of Rest–Activity Behavior by the Central Clock in Drosophila
Kumar, S., & Sehgal, A. (2014) · Springer eBooks · doi:10.1007/978-3-319-08945-4_3 · Cited by 1
Phenological Coadaptation Can Stabilize Predator–Prey Dynamics
Mougi, A. (2022) · Frontiers in Ecology and Evolution · doi:10.3389/fevo.2022.817339 · Cited by 1
“Because seasonal rhythms of biological activities and life history events are controlled by genetic factors (Bradshaw and Holzapfel, 2001; Réale et al., 2003; Tauber et al., 2007; van Asch et al., 2007; Liedvogel et al., 2009; Wilczek et al., 2010), phenology can change through the occurrence of microevolution and/or…”
Background
Genetic approaches to understanding circadian entrainment
Roenneberg, T., & Allebrandt, K. V. (2013) · Cambridge University Press eBooks · doi:10.1017/cbo9781139649469.018 · Cited by 1
Ending Diapause and Reinitiating Development
Denlinger, D. L. (2022) · Cambridge University Press eBooks · doi:10.1017/9781108609364.009 · Cited by 1
The genetics of adaptive photoperiodic response in Nasonia vitripennis
Paolucci, S. (2014) · University of Groningen research database (University of Groningen / Centre for Information Technology) · Cited by 1
Geographically patterned variation in diapause and its relationship to other climate-associated phenotypes and genotypes of Drosophila americana
Hart-Schmidt, R. A. (2012) · doi:10.17077/etd.76xs032s · Cited by 1
“The diapause cline in European D. melanogaster is associated with variation in timeless, with two alleles differentially interacting with photoperiod and 21 genetic background to produce seasonally appropriate diapause (Tauber et al 2007, Sandrelli et al 2007).”
BackgroundInfluential
Major changes in gene expression between strains of diapausing and non-diapause spruce budworm despite little evidence of genetic divergencePreprint
van der Burg, K. R. L., Gauthier, J., Roe, A. D., Cusson, M., Boyle, B., Lévesque, R. C., & Marshall, K. E. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.11.20.624545 · Cited by 1
Splicing of a core clock gene regulates seasonal adaptations by a winter gating mechanismPreprint
Hidalgo, S., Rio, R. D., Tabuloc, C. A., Hernandez, L. A. P., Berry, A. L., Cai, Y. D., Lewald, K. M., & Chiu, J. C. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.11.06.687099 · Cited by 1
The genetic basis of phenotypic plasticity in natural populations of Drosophila
O’Brien, K. R. (2014) · ScholarlyCommons (University of Pennsylvania)
Orientierung in Zeit und Raum
Kappeler, P. M. (2011) · Springer-Lehrbuch · doi:10.1007/978-3-642-20653-5_4
Sleepphysiology and homeostasis
Shaw, P. J., Tafti, M., & Thorpy, M. J. (2013) · Cambridge University Press eBooks · doi:10.1017/cbo9781139649469.016
Couch potato -kandidaattigeenissä esiintyvän mutaation vaikutus Drosophila montana -naaraiden lisääntymislepokauteen
Lampinen, H. (2010) · Jyväskylä University Digital Archive (University of Jyväskylä)
Evolution of Photoperiodism in the Threespine Stickleback Gasterosteus aculeatus
O’Brien, C. S. (2011) · Scholars' Bank (University of Oregon)
Для чого потрібні циркадні ритми, або як змінити хід «біологічного годинника»
Романюк, С. И., & Комісаренко, С. В. (2017) · Visnik Nacional noi academii nauk Ukrai ni · doi:10.15407/visn2017.12.050
Analyzing the neutral and adaptive background of butterfly voltinism reveals structural variation in a core circadian genePreprint
Lindestad, O., Nylin, S., Wheat, C. W., & Gotthard, K. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.05.13.093310
“In several cases (Tauber et al., 2007; Yamada & Yamamoto, 2011; Pruisscher et al., 2018; Dalla Benetta et al., 2019), the detected large-effect loci are components of the circadian clock, which exhibit a widely recognized, but controversial and poorly understood, link with photoperiodism across…”
Background
GENETIC VARIATION IN THE timeless GENE MEDIATES METABOLIC STATES OF Drosophila melanogaster IN RESPONSE TO PHOTOPERIOD
Belay, H. T. (2018) · TSpace (University of Toronto)
C O M M E N TA R Y Open Access
Bradshaw, W. E., & Holzapfel, C. M. (2010)
References
(2022) · Cambridge University Press eBooks · doi:10.1017/9781108609364.014
Evolution of Diapause
Denlinger, D. L. (2022) · Cambridge University Press eBooks · doi:10.1017/9781108609364.012
The Cost of Diapause and Some Diapause Alternatives
Denlinger, D. L. (2022) · Cambridge University Press eBooks · doi:10.1017/9781108609364.005
Subject Index
Denlinger, D. L. (2022) · Cambridge University Press eBooks · doi:10.1017/9781108609364.016
Genetic Control of Diapause
Denlinger, D. L. (2022) · Cambridge University Press eBooks · doi:10.1017/9781108609364.011
Variation in the Diapause Response
Denlinger, D. L. (2022) · Cambridge University Press eBooks · doi:10.1017/9781108609364.004
Wider Implications
Denlinger, D. L. (2022) · Cambridge University Press eBooks · doi:10.1017/9781108609364.013
Species Index
Denlinger, D. L. (2022) · Cambridge University Press eBooks · doi:10.1017/9781108609364.015
Preface
Denlinger, D. L. (2022) · Cambridge University Press eBooks · doi:10.1017/9781108609364.001
Plate Section (PDF Only)
Denlinger, D. L. (2022) · Cambridge University Press eBooks · doi:10.1017/9781108609364.017
Orientierung in Zeit und Raum
(2008) · Springer-Lehrbuch · doi:10.1007/978-3-540-68792-4_4
Orientierung in Zeit und Raum
Kappeler, P. M. (2016) · Springer eBooks · doi:10.1007/978-3-662-53145-7_4
TIMELESS CLOCK
Merzendorfer, H. (2007) · Journal of Experimental Biology · doi:10.1242/jeb.001180
Research Highlights
(2007) · Nature Genetics · doi:10.1038/ng0807-943
The circadian clock conveys thermal and photoperiodic cues to modulate EYES ABSENT via the neuropeptide PDF to regulate seasonal physiologyPreprint
Hidalgo, S., Anguiano, M., Tabuloc, C. A., & Chiu, J. C. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.10.27.514061
Mapping the Regulatory Architecture of Circadian Clock Adaptation: A Genome-Wide eQTL Analysis in Drosophila melanogasterPreprint
Yair, M., Fishman, B., Aslan, M., & Tauber, E. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.05.18.654706
“For instance, the insertion/deletion polymorphism in the tim gene of Drosophila results in two allelic forms ( ls-tim and s-tim ) with distinct light sensitivities and diapause behaviors, showing clinal distribution patterns across Europe that suggest directional selection (Tauber et al. 2007).”
The dynamic relationship between oogenesis and whole-animal physiology
Carvalho-Santos, Z. (2025) · Elsevier eBooks · doi:10.1016/b978-0-323-95424-2.00027-3 · Cited by 1
Circadian biology of songbirds : endogenous and environmental components
Lehmann, M. (2014) · KOPS (University of Konstanz)
Contrôle de la stabilité de TIMELESS par un complexe ubiquitine ligase de type Culline-3 dans l’horloge circadienne de Drosophila melanogaster
Dognon, A. (2011) · theses.fr (ABES) · doi:10.70675/0930003az6b9dz447ezad50zc93ffb258abd
“Quant à l’allèle s-tim, la délétion d’une guanine entre les deux codons d’initiation, interrompt la phase de lecture avec un codon stop, générant la forme S-TIM uniquement (Tauber et al., 2007 ; Sandrelli et al., 2007).”

Authors: Tauber, E., Zordan, M., Sandrelli, F., Pegoraro, M., Osterwalder, N., Breda, C., Daga, A., Selmin, A., Monger, K., Benna, C., Rosato, E., Kyriacou, C. P., & Costa, R.
Affiliations: University of Padua (IT)
Department of Genetics, University of Leicester, Leicester LE1 7RH, UK.
Corresponding author: Tauber, Eran
Zordan, Mauro
Sandrelli, Federica
Daga, Andrea
Kyriacou, Charalambos P.
ORCID: Tauber, Eran
Zordan, Mauro
Sandrelli, Federica
Pegoraro, Mirko
Breda, Carlo
Daga, Andrea
Benna, Clara
Rosato, Ezio
Kyriacou, Charalambos P.
Costa, Rodolfo
Venue: Science
Publisher: American Association for the Advancement of Science (AAAS)
Published: 2007-06-29
Volume: 316
Issue: 5833
Pages: 1895-1898
ISSN: 0036-8075 (ISSN-L)
1095-9203
DOI: 10.1126/science.1138412
OpenAlex: W2142166311
Cited by: 308
References: 23
Citations by year: 2026: 8 · 2025: 12 · 2024: 8 · 2023: 17 · 2022: 28 · 2021: 11 · 2020: 18 · 2019: 11 · 2018: 15 · 2017: 12 · 2016: 17 · 2015: 11 · 2014: 15 · 2013: 18 · 2012: 17
FWCI: 9.53
Type: journal article
Language: en
Open access: closed
Locations: Science (publishedVersion)
PubMed (publishedVersion)
Leicester Research Archive (University of Leicester) (submittedVersion)
Padua Research Archive (University of Padova) (submittedVersion)
Funders: Natural Environment Research Council (NE/D012058/1)
Topics: Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
Physical Sciences › Environmental Science › Ecology › Physiological and biochemical adaptations
Keywords: timeless gene, circadian clock, natural selection, diapause, life-history traits, seasonal adaptation, Drosophila melanogaster
MeSH terms: Alleles, Amino Acid Sequence, Animals, Base Sequence, Circadian Rhythm, Drosophila melanogaster, Europe, Female, Geography, Haplotypes, Molecular Sequence Data, Mutation, Phylogeny, Polymorphism, Genetic, Reproduction, Seasons, Selection, Genetic, Temperature, Transformation, Genetic, Photoperiod, Evolution, Molecular, Protein Isoforms, Drosophila Proteins

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Natural Selection Favors a Newly Derived timeless Allele in Drosophila melanogaster

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Citations

Cites

Cited by

Related

Metadata

Record

About these checks