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The genomic basis of circadian and circalunar timing adaptations in a midge
Open accessAbstract
Organisms use endogenous clocks to anticipate regular environmental cycles, such as days and tides. Natural variants resulting in differently timed behaviour or physiology, known as chronotypes in humans, have not been well characterized at the molecular level. We sequenced the genome of Clunio marinus, a marine midge whose reproduction is timed by circadian and circalunar clocks. Midges from different locations show strain-specific genetic timing adaptations. We examined genetic variation in five C. marinus strains from different locations and mapped quantitative trait loci for circalunar and circadian chronotypes. The region most strongly associated with circadian chronotypes generates strain-specific differences in the abundance of calcium/calmodulin-dependent kinase II.1 (CaMKII.1) splice variants. As equivalent variants were shown to alter CaMKII activity in Drosophila melanogaster, and C. marinus (Cma)-CaMKII.1 increases the transcriptional activity of the dimer of the circadian proteins Cma-CLOCK and Cma-CYCLE, we suggest that modulation of alternative splicing is a mechanism for natural adaptation in circadian timing.
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“Interestingly, one of the two quantitative trait loci (QTLs) linked to circalunar timing overlaps largely with one of the two circadian QTLs [46]”
From The Still Dark Side of the Moon: Molecular Mechanisms of Lunar-Controlled Rhythms and Clocks (2020) · cites this paper as [46]
In the citing paper
“However, the mapping of all known genes with key roles in circadian timing or light input pathways revealed their complete absence from these QTLs [46]”
From The Still Dark Side of the Moon: Molecular Mechanisms of Lunar-Controlled Rhythms and Clocks (2020) · cites this paper as [46]
In the citing paper
“Genetic linkage analysis identified two specific chromosomal regions responsible for diurnal emergence and two related to lunar timing.”
From The Still Dark Side of the Moon: Molecular Mechanisms of Lunar-Controlled Rhythms and Clocks (2020) · cites this paper as [46]
In the citing paper
“Interestingly, the current analysis in the midge is consistent with the idea that circadian and circalunar timing mechanisms are distinct, as none of the core circadian clock genes is involved in circalunar timing variation (29).”
From An Overview of Monthly Rhythms and Clocks (2017) · cites this paper as [29]
In the citing paper
“Combining rigorous genetic mapping of these differences with a high-resolution genome for this insect, as well as re-sequencing of distinct chronotypes, has recently allowed the identification of several candidate genes modulating circalunar (and circadian) timing in distinct C. marinus timing strains (29).”
From An Overview of Monthly Rhythms and Clocks (2017) · cites this paper as [29]
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Self-citationLunar cycle-mediated behaviours in animals, including humans
Mandal, F. B. (2023) · Israel Journal of Ecology and Evolution · doi:10.1163/22244662-bja10060 · Cited by 3
Chronobiology as compensation: can biological rhythms compensate for sexual signals?
Westwood, M. L., Broder, E. D., Welsh, G. T., & Tinghitella, R. M. (2025) · Frontiers in Ethology · doi:10.3389/fetho.2024.1473358 · Cited by 2
Martin, S. L. F., Torre, R. L., Danneels, B., Tooming‐Klunderud, A., Skage, M., Kollias, S., Tørresen, O. K., Falahati‐Anbaran, M., Stur, E., Jakobsen, K. S., et al. (2025) · GigaScience · doi:10.1093/gigascience/giaf160 · Cited by 1
Ando, H. (2018) · Hikaku seiri seikagaku(Comparative Physiology and Biochemistry) · doi:10.3330/hikakuseiriseika.35.45 · Cited by 2
On the fitness of informative cues in complex environments
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Michailova, P., Kovalenko, P. A., Serga, S. V., Parnikoza, I., Kozeretska, I. A., & Convey, P. (2023) · Antarctic Science · doi:10.1017/s0954102023000202 · Cited by 1
Seasonal Dynamics of Non-Biting Midges (Diptera: Chironomidae) and Relevant Environmental Factors
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How competition can drive allochronic divergence: A case study in the Marine Midge, Clunio marinus
Jacobsen, A. G. G., Kaiser, T. S., & Gokhale, C. S. (2026) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1014235 · Cited by 1
Self-citationFrontiers in Chronobiology: Endogenous Clocks at the Core of Signaling Pathways in Physiology
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Finch, G., Nandyal, S., Perrieta, C., Davies, B., Rosendale, A. J., Holmes, C. J., Gantz, J. D., Spacht, D. E., Bailey, S. T., Chen, X., et al. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/796797 · Cited by 2
Biological Clocks and Circadian Rhythms
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Phenological evolution on a cyclical Earth: towards first principles and null expectationsPreprint
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Kita, A., Elsayed, A. K., & Tokuda, M. (2022) · Biodiversity Data Journal · doi:10.3897/bdj.10.e79184
Metadata
- Authors
- Kaiser, T. S., Poehn, B., Szkiba, D., Preussner, M., Sedlazeck, F. J., Zrim, A., Neumann, T., Nguyen, L.-T., Betancourt, A. J., Hummel, T., Vogel, H., Dorner, S., Heyd, F., von Haeseler, A., & Tessmar-Raible, K.
- Affiliations
- University of Vienna (AT)
- Freie Universität Berlin (DE)
- University of Veterinary Medicine Vienna (AT)
- Max Planck Institute for Chemical Ecology (DE)
- Corresponding author
- Kaiser, Tobias S.
- ORCID
- Venue
- Nature
- Published
- 2016-11-21
- Volume
- 540
- Issue
- 7631
- Pages
- 69-73
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC5133387
- OpenAlex
- W2555773426
- Cited by
- 109
- References
- 74
- Citations by year
- 2026: 2 · 2025: 13 · 2024: 9 · 2023: 7 · 2022: 19 · 2021: 16 · 2020: 11 · 2019: 12 · 2018: 11 · 2017: 9
- FWCI
- 6.79
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Locations
- Nature (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
- RePEc: Research Papers in Economics (submittedVersion)
- Max Planck Digital Library (submittedVersion)
- Max Planck Digital Library (submittedVersion, other-oa)
- MPG.PuRe (Max Planck Society) (submittedVersion)
- Refubium (Universitätsbibliothek der Freien Universität Berlin) (submittedVersion, cc-by)
- Universitätsbibliothek der FU Berlin Hochschulschriftenstelle u. Dokumentenserver (cc-by)
- Funders
- Deutsche Forschungsgemeinschaft (FP7/2007–2013, HE5398/4)
- Austrian Science Fund (#AY0041321)
- Universität Wien (I059-N)
- FP7 Ideas: European Research Council (337011)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
- Physical Sciences › Environmental Science › Ecology › Physiological and biochemical adaptations
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
- Keywords
- Clunio marinus, circadian clock, chronotype, alternative splicing, calcium/calmodulin-dependent kinase II, quantitative trait loci, natural genetic variation, Drosophila melanogaster
- MeSH terms
- Acclimatization, Animals, Chironomidae, Circadian Rhythm, Drosophila melanogaster, Male, Phenotype, Reproduction, Species Specificity, Time Factors, Transcription, Genetic, Genetic Variation, Moon, Alternative Splicing, Genomics, Quantitative Trait Loci, Genome, Insect, Calcium-Calmodulin-Dependent Protein Kinase Type 2, Tidal Waves, Genetic Association Studies, CLOCK Proteins, Circadian Clocks
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