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Natural Selection Favors a Newly Derived timeless Allele in Drosophila melanogaster
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.
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“For example, Drosophila melanogaster that is native to Europe harbors a polymorphism in “timeless,” a key gene in the light response of the circadian system, that follows a latitudinal cline in allele frequency (Sandrelli et al. 2007; Tauber et al. 2007).”
From Archaic Introgression Shaped Human Circadian Traits (2023) · cites this paper as Tauber et al. 2007
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“In addition, there is a latitudinal cline in genetic tendency to diapause among populations of D. melanogaster (Schmidt et al. 2005; Tauber et al. 2007) and a Dutch population of D. melanogaster has a longer critical photoperiod than Italian populations (Tauber et al. 2007).”
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“…as well, including timeless (tim), timeout and cryptochrome (cry), which have all previously been found to vary clinally (Sandrelli et al. 2007; Tauber et al. 2007; Turner et al. 2008; Kolaczkowski et al. 2011), as well as a novel clinal candidate, clock (Clk) (Appendix S10, Supporting…”
BackgroundFlatt, T., & Heyland, A. (2011) · Cited by 256
Light, Time, and the Physiology of Biotic Response to Rapid Climate Change in Animals
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“ls-tim produces a long and short TIM isoform, whereas s-tim generates the shorter isoform only [60].”
BackgroundInfluentialSelf-citationSetting the clock – by nature: Circadian rhythm in the fruitfly Drosophila melanogaster
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“Another way of fine-tuning circadian photoreception was revealed in several recent publications [52,57,58].”
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“It has been reported that TIM (Tauber et al. 2007) and DM (Jensen et al.”
BackgroundInfluentialPeschel, N., Chen, K., Szabo, G., & Stanewsky, R. (2009) · Current Biology · doi:10.1016/j.cub.2008.12.042 · Cited by 215
Kolaczkowski, B., Kern, A. D., Holloway, A. K., & Begun, D. J. (2010) · Genetics · doi:10.1534/genetics.110.123059 · Cited by 212
“…gene, which regulates circadian rhythm, is highly differentiated (FST¼ 0.30), as are couch potato (FST ¼ 0.23) and timeless (FST ¼ 0.20), which have already been implicated in spatially varying selection in D. melanogaster (Sandrelli et al. 2007; Tauber et al. 2007; Schmidt et al. 2008).”
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Ikeno, T., Tanaka, S., Numata, H., & Goto, S. G. (2010) · BMC Biology · doi:10.1186/1741-7007-8-116 · Cited by 211
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BackgroundA Molecular Basis for Natural Selection at the timeless Locus in Drosophila melanogaster
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“(36) showed that in three populations there was a significant relationship between the proportion expressing diapause, the testing photoperiod, and homozygous genotypes for the timeless alleles s-tim and ls-tim.”
BackgroundEmerson, K. J., Bradshaw, W. E., & Holzapfel, C. M. (2009) · Trends in Genetics · doi:10.1016/j.tig.2009.03.009 · Cited by 197
“In both Italian and Dutch populations, there is a linear decline in the incidence of diapause with increasing day length and, at each day length, the incidence of diapause is greater in ls-tim than in s-tim flies [ 44 ].”
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Climate change-driven species' range shifts filtered by photoperiodism
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“melanogaster that are exposed to seasonal changes in environmental conditions enter an adaptive state referred to as diapause [9,14,90,91,92].”
BackgroundEvolutionary Links Between Circadian Clocks and Photoperiodic Diapause in Insects
Meuti, M. E., & Denlinger, D. L. (2013) · Integrative and Comparative Biology · doi:10.1093/icb/ict023 · Cited by 155
“Two naturally varying alleles of tim are present in D. melanogaster (Tauber et al. 2007); one that exclusively produces a short form of the mRNA (s-tim) and one that produces both long and short forms (ls-tim).”
BackgroundInfluentialClines in clock genes: fine-tuning circadian rhythms to the environment
Kyriacou, C. P., Peixoto, A. A., Sandrelli, F., Costa, R., & Tauber, E. (2008) · Trends in Genetics · doi:10.1016/j.tig.2007.12.003 · Cited by 154
“Redrawn from Tauber et al., (2007) [13].”
MethodRhythm Defects Caused by Newly Engineered Null Mutations in Drosophila's cryptochrome Gene
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“The utility of this interlocus contrast has been effectively demonstrated in Drosophila where latitudinal clines for candidate genes appear to be the rule rather than the exception (Berry and Kreitman 1993, Schmidt et al. 2000b, Gockel et al. 2001, Sezgin et al. 2004, Tauber et al. 2007).”
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“melanogaster (Tauber et al., 2007) and Chymomyza costata (Stehlik et al.”
BackgroundKapun, M., Barrón, M. G., Staubach, F., Obbard, D. J., Wiberg, R. A. W., Vieira, J., Goubert, C., Rota‐Stabelli, O., Kankare, M., Bogaerts-Márquez, M., et al. (2020) · Molecular Biology and Evolution · doi:10.1093/molbev/msaa120 · Cited by 150
“latitudinal cline in reproductive dormancy in North America (Tauber et al. 2007; Schmidt et al. 2008; Fabian et al. 2012).”
BackgroundBajgar, A., Jindra, M., & Doležel, D. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1217060110 · Cited by 143
“melanogaster (25, 26), and diapause in another drosophilid fly, Chymomyza costata, is altered by a timeless mutation (27, 28).”
BackgroundUnderstanding systems-level properties: timely stories from the study of clocks
Hogenesch, J. B., & Ueda, H. R. (2011) · Nature Reviews Genetics · doi:10.1038/nrg2972 · Cited by 136
Comparative analysis of circadian clock genes in insects
Sandrelli, F., Costa, R., Kyriacou, C. P., & Rosato, E. (2008) · Insect Molecular Biology · doi:10.1111/j.1365-2583.2008.00832.x · Cited by 134
“The long standing debate on whether clock genes can contribute to photoperiodic diapause in insects (Nunes & Saunders, 1999; Bradshaw et al., 2006) has been further stoked by the findings that in D. melanogaster, a new tim natural variant, ls-tim appears to be under natural selection because it enhances the level of d…”
BackgroundResultInfluentialThe influence of biological rhythms on host–parasite interactions
Martinez, M. E., & Helm, B. (2015) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2015.03.012 · Cited by 135
Bloch, G., Barnes, B. M., Gerkema, M. P., & Helm, B. (2013) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2013.0019 · Cited by 135
“Genetic data further indicate that natural selection acts on clock-gene variants [8], but the precise fitness benefits of circadian clocks for wild organisms are still largely unclear [4,9].”
BackgroundWhat Season Is It Anyway? Circadian Tracking vs. Photoperiodic Anticipation in Insects
Bradshaw, W. E., & Holzapfel, C. M. (2010) · Journal of Biological Rhythms · doi:10.1177/0748730410365656 · Cited by 132
“melanogaster (Tauber et al., 2007; Sandrelli et al., 2007) and point out, correctly, that the effect of this massive timeless mutation in C.”
BackgroundInfluentialRoles of circadian clock genes in insect photoperiodism
Goto, S. G. (2012) · Entomological Science · doi:10.1111/ens.12000 · Cited by 131
“Based on Tauber et al. (2007). Circadian clock genes and photoperiodism”
BackgroundModel and Non-model Insects in Chronobiology
Beer, K., & Helfrich‐Förster, C. (2020) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2020.601676 · Cited by 125
A Plastic Clock: How Circadian Rhythms Respond to Environmental Cues in Drosophila
Dubruille, R., & Emery, P. (2008) · Molecular Neurobiology · doi:10.1007/s12035-008-8035-y · Cited by 124
“In this variant, the presence of two alternative start codons results in expression of a long and a short form of TIM [79–81].”
BackgroundOn the Adaptive Significance of Circadian Clocks for Their Owners
Vaze, K. M., & Sharma, V. K. (2013) · Chronobiology International · doi:10.3109/07420528.2012.754457 · Cited by 124
“Functional analysis of tim polymorphism revealed a causal role of tim alleles in the regulation of incidence of ovarian diapause (Tauber et al., 2007). ls-tim, which is predominant in southern Europe, showed higher incidence of diapause than stim genotypes.”
BackgroundInfluentialGenetic Differences in Human Circadian Clock Genes among Worldwide Populations
Ciarleglio, C. M., Ryckman, K. K., Servick, S. V., Hida, A., Robbins, S., Wells, N., Hicks, J., Larson, S. A., Wiedermann, J. P., Carver, K., et al. (2008) · Journal of Biological Rhythms · doi:10.1177/0748730408320284 · Cited by 123
“In particular, our data do not support selection of clock gene alleles on the basis of latitude/photoperiod, which might be predicted to affect the evolution of circadian clock genes (as in Drosophila; Sawyer et al., 2006; Tauber et al., 2007).”
BackgroundResultInfluentialSeasonal variation in life history traits in two Drosophila species
Behrman, E. L., Watson, S. S., O’Brien, K. R., Heschel, M. S., & SCHMIDT, P. S. (2015) · Journal of Evolutionary Biology · doi:10.1111/jeb.12690 · Cited by 122
“…young sample, the age composition followed the predicted increase in heterogeneity as the population grew and reproduced throughout the summer (Tauber et al., 1986); such seasonal changes in population age composition have also been documented in the medfly Ceratitis capitata (Carey et al.,…”
BackgroundPoelchau, M. F., Reynolds, J. A., Denlinger, D. L., Elsik, C. G., & Armbruster, P. (2011) · BMC Genomics · doi:10.1186/1471-2164-12-619 · Cited by 120
“A classic hypothesis proposes that circadian rhythm underlies the expression of photoperiodic diapause [58], although evidence supporting this hypothesis is limited [59,60] and highly debated [e.”
BackgroundLife-History Evolution and the Polyphenic Regulation of Somatic Maintenance and Survival
Flatt, T., Amdam, G. V., Kirkwood, T. B. L., & Omholt, S. W. (2013) · The Quarterly Review of Biology · doi:10.1086/671484 · Cited by 114
“The third candidate gene found to affect dormancy in natural populations, timeless (tim), does not seem to be directly involved in the endocrine control of dormancy, but probably plays a role in its photoperiodic regulation (Sandrelli et al. 2007; Tauber et al. 2007; Emerson et al. 2009a; Schiesari et al. 2011; Schmid…”
BackgroundO'Malley, K. G., & Banks, M. A. (2008) · Proceedings of the Royal Society B: Biological Sciences · doi:10.1098/rspb.2008.0524 · Cited by 111
Dissecting the genetics of longevity inDrosophila melanogaster
Paaby, A. B., & SCHMIDT, P. S. (2009) · Fly · doi:10.4161/fly.3.1.7771 · Cited by 100
Stehlík, J., Závodská, R., Shimada, K., Šauman, I., & Košťál, V. (2008) · Journal of Biological Rhythms · doi:10.1177/0748730407313364 · Cited by 98
“melanogaster and pitcherplant mosquito indicated that although circadian clocks and photoperiodic calendar appear as genetically distinct mechanisms/processes, the clock gene timeless (tim) may affect the incidence of diapause directly, independently of its function in the central circadian oscillator (Mathias et al.,…”
BackgroundKučerová, L., Kubrak, O. I., Bengtsson, J., Strnad, H., Nylin, S., Theopold, U., & Nässel, D. R. (2016) · BMC Genomics · doi:10.1186/s12864-016-2383-1 · Cited by 97
“[147] provided evidence that a mutation in the clock gene timeless has spread in Europe over the last 10 000 years, and suggested a link to an enhancement of diapause (see also [148]).”
BackgroundGenomic Basis of Circannual Rhythm in the European Corn Borer Moth
Kozak, G. M., Wadsworth, C. B., Kahne, S. C., Bogdanowicz, S. M., Harrison, R. G., Coates, B. S., & Dopman, E. B. (2019) · Current Biology · doi:10.1016/j.cub.2019.08.053 · Cited by 94
Saunders, D. S., & Bertossa, R. C. (2011) · Journal of Insect Physiology · doi:10.1016/j.jinsphys.2011.01.013 · Cited by 94
Shiga, S., & Numata, H. (2009) · Journal of Experimental Biology · doi:10.1242/jeb.027003 · Cited by 94
“melanogaster have suggested that tim directly affects the incidence of diapause through circadian photoreception (Tauber et al., 2007; Sandrelli et al., 2007).”
BackgroundBaker, D. A., & Russell, S. R. H. (2009) · BMC Genomics · doi:10.1186/1471-2164-10-242 · Cited by 94
“melanogaster displaying circadian induced reproductive arrest under laboratory conditions [8] and over environmental clines [9,10].”
BackgroundSakamoto, T., Uryu, O., & Tomioka, K. (2009) · Journal of Biological Rhythms · doi:10.1177/0748730409341523 · Cited by 91
“Due to the reduced photosensitivity of the circadian clock, flies carrying ls-tim have a longer critical photoperiod for an ovarian diapause (Tauber et al., 2007).”
BackgroundAbrieux, A., Xue, Y., Cai, Y. D., Lewald, K. M., Nguyen, H. N., Zhang, Y., & Chiu, J. C. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2004262117 · Cited by 89
The Circadian Clock of the Fly: A Neurogenetics Journey Through Time
Özkaya, Ö., & Rosato, E. (2012) · Advances in genetics · doi:10.1016/b978-0-12-387687-4.00004-0 · Cited by 86
“An insertion/deletion polymorphism found in the tim locus of natural populations can generate two forms of the TIM protein that differ at the N-terminus for the presence (the long form) or absence (the short form) of 23 amino acids (Rosato et al., 1997; Sandrelli et al., 2007; Tauber et al., 2007).”
BackgroundThe search for circadian clock components in humans: new perspectives for association studies
Allebrandt, K. V., & Roenneberg, T. (2008) · Brazilian Journal of Medical and Biological Research · doi:10.1590/s0100-879x2008000800013 · Cited by 84
“Latitudinal clines related to human reproduction (43,44), human mortality (45) or genetic geographic variations between photoperiodic diapauses and the circadian eclosion rhythm in Drosophila (46-49) have been observed.”
BackgroundEvolutionary and functional genetics of insect diapause: a call for greater integration
Ragland, G. J., Armbruster, P., & Meuti, M. E. (2019) · Current Opinion in Insect Science · doi:10.1016/j.cois.2019.08.003 · Cited by 83
“[21] identified genetic variants of timeless in isofemale lines varying in diapause incidence.”
BackgroundThe hormonal and circadian basis for insect photoperiodic timing
Schiesari, L., Kyriacou, C. P., & Costa, R. (2011) · FEBS Letters · doi:10.1016/j.febslet.2011.02.026 · Cited by 82
“show a different photoperiodism, in that the slopes of the photoperiodic component of diapause are the same [138] (Fig.”
BackgroundInfluentialComparative transcriptomics support evolutionary convergence of diapause responses across I nsecta
Ragland, G. J., & Keep, E. (2017) · Physiological Entomology · doi:10.1111/phen.12193 · Cited by 84
“In addition, allelic variants of tim vary predictably with geography and associate with propensity to enter diapause in D. melanogaster (Sandrelli et al., 2007; Tauber et al., 2007).”
BackgroundGenetic variation underlying local adaptation of diapause induction along a cline in a butterfly
Pruisscher, P., Nylin, S., Gotthard, K., & Wheat, C. W. (2018) · Molecular Ecology · doi:10.1111/mec.14829 · Cited by 83
“melanogaster, where different timeless variants in a latitudinal cline affected photoperiodically induced quiescence, which was modified by the genetic background (Tauber et al., 2007).”
BackgroundDrosophila timeless2 Is Required for Chromosome Stability and Circadian Photoreception
Benna, C., Bonaccorsi, S., Wülbeck, C., Helfrich‐Förster, C., Gatti, M., Kyriacou, C. P., Costa, R., & Sandrelli, F. (2010) · Current Biology · doi:10.1016/j.cub.2009.12.048 · Cited by 82
“We initially determined the ls-tim1/s-tim1 genotype of each strain, because this natural tim1 polymorphism significantly affects the circadian light response (Table S2) [31–34].”
Common features in diverse insect clocks
Numata, H., Miyazaki, Y., & Ikeno, T. (2015) · Zoological Letters · doi:10.1186/s40851-014-0003-y · Cited by 83
“induction of diapause [135,136].”
Kankare, M., Salminen, T., Laiho, A., Vesala, L., & Hoikkala, A. (2010) · BMC Ecology · doi:10.1186/1472-6785-10-3 · Cited by 65
“D. melanogaster females are known to enter adult reproductive diapause in response to short days and low temperatures in Europe [11] and in North America [10,12].”
Emerson, K. J., Bradshaw, W. E., & Holzapfel, C. M. (2010) · PLoS ONE · doi:10.1371/journal.pone.0009574 · Cited by 79
“As a consequence of wide acceptance of Bünning’s [17] hypothesis that daily circadian rhythms form the necessary, causal basis of the seasonal photoperiodic switch, candidate gene-based studies of the photoperiodic switch have emphasized known circadian rhythm genes [18–23].”
BackgroundPeptidergic signaling from clock neurons regulates reproductive dormancy in Drosophila melanogaster
Nagy, D., Cusumano, P., Andreatta, G., Anduaga, A. M., Hermann-Luibl, C., Reinhard, N., Gesto, J. S. M., Wegener, C., Mazzotta, G. M., Rosato, E., et al. (2019) · PLoS Genetics · doi:10.1371/journal.pgen.1008158 · Cited by 77
Ikeno, T., Numata, H., & Goto, S. G. (2008) · Gene · doi:10.1016/j.gene.2008.05.002 · Cited by 76
Adaptation of Circadian Neuronal Network to Photoperiod in High-Latitude European Drosophilids
Menegazzi, P., Benetta, E. D., Beauchamp, M., Schlichting, M., Steffan-Dewenter, I. D., & Helfrich‐Förster, C. (2017) · Current Biology · doi:10.1016/j.cub.2017.01.036 · Cited by 74
Erickson, P. A., Weller, C. A., Song, D., Bangerter, A. S., SCHMIDT, P. S., & Bergland, A. O. (2020) · PLoS Genetics · doi:10.1371/journal.pgen.1009110 · Cited by 70
“599 melanogaster, which has previously been characterized as being under the control of a 600 small number of loci with large effect using QTL mapping and candidate gene 601 approaches [27,52,60,76].”
BackgroundGenetic dissection of stress-induced reproductive arrest in Drosophila melanogaster females
Ojima, N., Hara, Y., Ito, H., & Yamamoto, D. (2018) · PLoS Genetics · doi:10.1371/journal.pgen.1007434 · Cited by 72
Environmental control of ovarian dormancy in natural populations of Drosophila melanogaster
Emerson, K. J., Uyemura, A. M., McDaniel, K. L., SCHMIDT, P. S., Bradshaw, W. E., & Holzapfel, C. M. (2009) · Journal of Comparative Physiology A · doi:10.1007/s00359-009-0460-5 · Cited by 70
“been evaluated only in European populations and then only at a single temperature ( Tauber et al. 2007 ).”
BackgroundMethodResultInfluentialDrosophila Clock Neurons under Natural Conditions
Menegazzi, P., Vanin, S., Yoshii, T., Rieger, D., Hermann, C., Dusik, V., Kyriacou, C. P., Helfrich‐Förster, C., & Costa, R. (2013) · Journal of Biological Rhythms · doi:10.1177/0748730412471303 · Cited by 69
“The photoperiodic and thermal stimuli that generate diapause are not well understood (Schiesari et al., 2011), although natural variants of TIM play a significant role (Tauber et al., 2007; Sandrelli et al., 2007).”
BackgroundGlobal Transcriptional Profiling of Diapause and Climatic Adaptation inDrosophila melanogaster
Zhao, X., Bergland, A. O., Behrman, E. L., Gregory, B. D., Petrov, D. A., & SCHMIDT, P. S. (2015) · Molecular Biology and Evolution · doi:10.1093/molbev/msv263 · Cited by 68
“Similarly, two major pathways have been implicated in diapause expression: The circadian clock (Tauber et al. 2007; Pegoraro et al. 2014) and insulin/insulin-like growth factor signaling (IIS) that plays a central role in the neuroendocrine regulation (Tatar, Kopelman, et al.”
BackgroundAminergic Signaling Controls Ovarian Dormancy in Drosophila
Andreatta, G., Kyriacou, C. P., Flatt, T., & Costa, R. (2018) · Scientific Reports · doi:10.1038/s41598-018-20407-z · Cited by 70
Identification and characterization of circadian clock genes in the pea aphid Acyrthosiphon pisum
Cortes, T., Ortiz-Rivas, B., & Martínez‐Torres, D. (2010) · Insect Molecular Biology · doi:10.1111/j.1365-2583.2009.00931.x · Cited by 66
“…genetic variation at the period and timeless loci in Drosophila producing latitudinal clines which are usually interpreted as evidence of adaptation to seasonal conditions at different latitudes (Costa et al., 1992; Sandrelli et al., 2007; Tauber et al., 2007; reviewed in Kyriacou et al., 2007).”
Association between Circadian Clock Genes and Diapause Incidence in Drosophila triauraria
Yamada, H., & Yamamoto, M. (2011) · PLoS ONE · doi:10.1371/journal.pone.0027493 · Cited by 66
“Furthermore, recent studies suggest non-clock functions of circadian clock genes in the diapause occurrence [40,41].”
BackgroundResultControversial aspects of photoperiodism in insects and mites
Saunders, D. S. (2010) · Journal of Insect Physiology · doi:10.1016/j.jinsphys.2010.05.002 · Cited by 65
“In recent years a number of investigations into the photoperiodic phenomenon have been conducted at the molecular and genetic levels (e.g. Doležel et al., 2005; Emerson et al., 2009; Pavelka et al., 2003; Tauber et al., 2007).”
BackgroundPhotoperiod affects compensating developmental rate across latitudes in the damselfly Lestes sponsa
Śniegula, S., & Johansson, F. (2010) · Ecological Entomology · doi:10.1111/j.1365-2311.2009.01164.x · Cited by 63
“Interestingly a few studies have found genetic differences among populations in their response to photoperiod, such that those living at northern and southern latitudes respectively have adapted their photoperiod responses to the light conditions at their latitudes (McWatters & Saunders, 1998; Bradshaw & Holzapfel, 20…”
BackgroundBenetta, E. D., Beukeboom, L. W., & van de Zande, L. (2019) · The American Naturalist · doi:10.1086/703159 · Cited by 63
Paolucci, S., Salis, L., Vermeulen, C. J., Beukeboom, L. W., & van de Zande, L. (2016) · Molecular Ecology · doi:10.1111/mec.13802 · Cited by 61
“Clinal variation in clock genes has previously been found in Drosophila melanogaster (Costa et al. 1992; Sawyer et al. 1997; Tauber et al. 2007; Fabian et al. 2012) and in the European corn borer moth Ostrinia nubilalis (Levy et al.”
BackgroundThe Insulin-Like Proteins dILPs-2/5 Determine Diapause Inducibility in Drosophila
Schiesari, L., Andreatta, G., Kyriacou, C. P., O’Connor, M. B., & Costa, R. (2016) · PLoS ONE · doi:10.1371/journal.pone.0163680 · Cited by 62
Is diapause an ancient adaptation in Drosophila ?
Zonato, V., Collins, L., Pegoraro, M., Tauber, E., & Kyriacou, C. P. (2017) · Journal of Insect Physiology · doi:10.1016/j.jinsphys.2017.01.017 · Cited by 62
“A natural polymorphism at the timeless (tim) locus also has a major effect on diapause induction (Tauber et al., 2007; Sandrelli et al., 2007).”
InfluentialRole for Circadian Clock Genes in Seasonal Timing: Testing the Bünning Hypothesis
Pegoraro, M., Gesto, J. S. M., Kyriacou, C. P., & Tauber, E. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004603 · Cited by 62
“In Drosophila triauraria , genetic variation in tim and cry (but not in per , Clk or cyc ) was significantly associated with the photoperiodic response [18].”
BackgroundMethodInfluentialCircadian clock genes, ovarian development and diapause
Bradshaw, W. E., & Holzapfel, C. M. (2010) · BMC Biology · doi:10.1186/1741-7007-8-115 · Cited by 60
Dowle, E. J., Powell, T. H. Q., Doellman, M. M., Meyers, P. J., Calvert, M. B., Walden, K. K. O., Robertson, H. M., Berlocher, S. H., Feder, J. L., Hahn, D. A., et al. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2002357117 · Cited by 60
“Variation in one or a few key regulatory genes can serve as the genetic substrate for phenotypic innovations that promote local adaptation of phenology (15, 16).”
BackgroundFabian, D. K., Lack, J., Mathur, V. S., Schlötterer, C., SCHMIDT, P. S., Pool, J. E., & Flatt, T. (2015) · Journal of Evolutionary Biology · doi:10.1111/jeb.12607 · Cited by 57
“The results further suggest a limited phenotypic influence of admixture from non-African temperate populations, which are known to have diapause ability (Saunders et al., 1989; Tauber et al., 2007; Schmidt & Paaby, 2008).”
Diapause in Drosophila melanogaster – Photoperiodicity, cold tolerance and metabolites
Anduaga, A. M., Nagy, D., Costa, R., & Kyriacou, C. P. (2018) · Journal of Insect Physiology · doi:10.1016/j.jinsphys.2018.01.003 · Cited by 58
Photoperiodic time measurement, photoreception, and circadian clocks in insect photoperiodism
Goto, S. G. (2022) · Applied Entomology and Zoology · doi:10.1007/s13355-022-00785-7 · Cited by 58
Green, E. W., O’Callaghan, E. K., Hansen, C. N., Bastianello, S., Bhavnani, S., Vanin, S., Armstrong, J. D., Costa, R., & Kyriacou, C. P. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1506093112 · Cited by 58
“Congenic male per, per, and per mutants were backcrossed for six generations to a w(1118) that had itself been previously backcrossed for 10 generations to the wild HU strain, isolated from the Netherlands in 2005, and maintained as isofemale lines (30).”
BackgroundOne phase of the dormancy developmental pathway is critical for the evolution of insect seasonality
Wadsworth, C. B., Woods, W. A., Hahn, D. A., & Dopman, E. B. (2013) · Journal of Evolutionary Biology · doi:10.1111/jeb.12227 · Cited by 57
“Variation in clock genes (Tauber et al., 2007), insulin signalling (Williams et al., 2006), couch potato (Schmidt et al., 2008) and other loci provide needed clarity on life-history evolution.”
BackgroundMenegazzi, P., Yoshii, T., & Helfrich‐Förster, C. (2012) · Journal of Biological Rhythms · doi:10.1177/0748730412463181 · Cited by 56
“Materials and Methods Fly strains CantonS and wild-type Alto-Adige (WTALA) flies (Sandrelli et al., 2007; Tauber et al., 2007) were used as the wild-type flies.”
MethodInsects at not so low temperature: Climate change in the temperate zone and its biotic consequences
Bradshaw, W. E., & Holzapfel, C. M. (2010) · Cambridge University Press eBooks · doi:10.1017/cbo9780511675997.011 · Cited by 55
Metadata
- 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
- Venue
- Science
- Published
- 2007-06-29
- Volume
- 316
- Issue
- 5833
- Pages
- 1895-1898
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- 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
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