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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Drosophila melanogaster native to Europe harbors a polymorphism in timeless that follows a latitudinal cline in allele frequency.
“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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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 · see citing works
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 · see citing works
Controversial 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 · see citing works
Photoperiod 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 · see citing works
Benetta, E. D., Beukeboom, L. W., & van de Zande, L. (2019) · The American Naturalist · doi:10.1086/703159 · Cited by 63 · see citing works
Paolucci, S., Salis, L., Vermeulen, C. J., Beukeboom, L. W., & van de Zande, L. (2016) · Molecular Ecology · doi:10.1111/mec.13802 · Cited by 62 · see citing works
The 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 · see citing works
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 · see citing works
Role 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 · see citing works
Circadian 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 · see citing works
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 · see citing works
Fabian, D., Lack, J., Mathur, V., Schlötterer, C., Schmidt, P., Pool, J., & Flatt, T. (2015) · Journal of Evolutionary Biology · doi:10.1111/jeb.12607 · Cited by 62 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
One 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 · see citing works
Menegazzi, P., Yoshii, T., & Helfrich‐Förster, C. (2012) · Journal of Biological Rhythms · doi:10.1177/0748730412463181 · Cited by 56 · see citing works
Insects 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 · see citing works
- 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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