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HomeNatureCircadian plasticity evolves through regulatory changes in a neuropeptide gene

Circadian plasticity evolves through regulatory changes in a neuropeptide gene

  • Rieger, D., Stanewsky, R. & Helfrich-Forster, C. Cryptochrome, compound eyes, Hofbauer-Buchner eyelets, and ocelli play different roles in the entrainment and masking pathway of the locomotor activity rhythm in the fruit fly Drosophila melanogaster. J. Biol. Rhythms 18, 377–391 (2003).

    CAS 

    Google Scholar
     

  • Auer, T. O., Shahandeh, M. P. & Benton, R. Drosophila sechellia: a genetic model for behavioral evolution and neuroecology. Annu. Rev. Genet. 55, 527–554 (2021).

    CAS 

    Google Scholar
     

  • Roca, I. T. et al. Shifting song frequencies in response to anthropogenic noise: a meta-analysis on birds and anurans. Behav. Ecol. 27, 1269–1274 (2016).


    Google Scholar
     

  • Caldwell, A. J., While, G. M. & Wapstra, E. Plasticity of thermoregulatory behaviour in response to the thermal environment by widespread and alpine reptile species. Anim. Behav. 132, 217–227 (2017).


    Google Scholar
     

  • Muraro, N. I., Pirez, N. & Ceriani, M. F. The circadian system: plasticity at many levels. Neuroscience 247, 280–293 (2013).

    CAS 

    Google Scholar
     

  • Wang, G. et al. Clock genes and environmental cues coordinate Anopheles pheromone synthesis, swarming, and mating. Science 371, 411–415 (2021).

    ADS 
    CAS 
    PubMed Central 

    Google Scholar
     

  • Horn, M. et al. The circadian clock improves fitness in the fruit fly, Drosophila melanogaster. Front. Physiol. 10, 1374 (2019).

    PubMed Central 

    Google Scholar
     

  • Hardeland, R. & Stange, G. Comparative studies on the circadian rhythms of locomotor activity of 40 Drosophila species. J. Interdiscipl. Cycle Res. 4, 353–359 (1973).


    Google Scholar
     

  • Rieger, D., Peschel, N., Dusik, V., Glotz, S. & Helfrich-Forster, C. The ability to entrain to long photoperiods differs between 3 Drosophila melanogaster wild-type strains and is modified by twilight simulation. J. Biol. Rhythms 27, 37–47 (2012).

    CAS 

    Google Scholar
     

  • Beauchamp, M. et al. Closely related fruit fly species living at different latitudes diverge in their circadian clock anatomy and rhythmic behavior. J. Biol. Rhythms 33, 602–613 (2018).


    Google Scholar
     

  • Bywalez, W. et al. The dual-oscillator system of Drosophila melanogaster under natural-like temperature cycles. Chronobiol. Int. 29, 395–407 (2012).


    Google Scholar
     

  • Matute, D. R., Gavin-Smyth, J. & Liu, G. Variable post-zygotic isolation in Drosophila melanogaster/D. simulans hybrids. J. Evol. Biol. 27, 1691–1705 (2014).

    CAS 

    Google Scholar
     

  • Lachaise, D. et al. in Historical Biogeography of the Drosophila melanogaster Species Subgroup (eds. Hecht, M. K., Wallace, B. & Prance, G. T.) 159–225 (Plenum, 1988).

  • Dean, M. D. & Ballard, J. W. Linking phylogenetics with population genetics to reconstruct the geographic origin of a species. Mol. Phylogenet. Evol. 32, 998–1009 (2004).

    CAS 

    Google Scholar
     

  • Hardin, P. E. Molecular genetic analysis of circadian timekeeping in Drosophila. Adv. Genet. 74, 141–173 (2011).

    CAS 

    Google Scholar
     

  • Hermann-Luibl, C. & Helfrich-Forster, C. Clock network in Drosophila. Curr. Opin. Insect Sci. 7, 65–70 (2015).


    Google Scholar
     

  • Vaze, K. M. & Helfrich-Forster, C. The neuropeptide PDF is crucial for delaying the phase of Drosophila’s evening neurons under long Zeitgeber periods. J. Biol. Rhythms 36, 442–460 (2021).

    PubMed Central 

    Google Scholar
     

  • Yoshii, T. et al. The neuropeptide pigment-dispersing factor adjusts period and phase of Drosophila’s clock. J. Neurosci. 29, 2597–2610 (2009).

    CAS 
    PubMed Central 

    Google Scholar
     

  • Schlichting, M. et al. A neural network underlying circadian entrainment and photoperiodic adjustment of sleep and activity in Drosophila. J. Neurosci. 36, 9084–9096 (2016).

    CAS 
    PubMed Central 

    Google Scholar
     

  • Peschel, N., Chen, K. F., Szabo, G. & Stanewsky, R. Light-dependent interactions between the Drosophila circadian clock factors Cryptochrome, Jetlag, and Timeless. Curr. Biol. 19, 241–247 (2009).

    CAS 

    Google Scholar
     

  • Gunawardhana, K. L. & Hardin, P. E. VRILLE controls PDF neuropeptide accumulation and arborization rhythms in small ventrolateral neurons to drive rhythmic behavior in Drosophila. Curr. Biol. 27, 3442–3453 (2017).

    CAS 

    Google Scholar
     

  • Mezan, S., Feuz, J. D., Deplancke, B. & Kadener, S. PDF signaling is an integral part of the Drosophila circadian molecular oscillator. Cell. Rep. 17, 708–719 (2016).

    CAS 
    PubMed Central 

    Google Scholar
     

  • Grima, B., Chelot, E., Xia, R. & Rouyer, F. Morning and evening peaks of activity rely on different clock neurons of the Drosophila brain. Nature 431, 869–873 (2004).

    ADS 
    CAS 

    Google Scholar
     

  • Delventhal, R. et al. Dissection of central clock function in Drosophila through cell-specific CRISPR-mediated clock gene disruption. eLife 8, e48308 (2019).

    CAS 
    PubMed Central 

    Google Scholar
     

  • Stoleru, D., Peng, Y., Agosto, J. & Rosbash, M. Coupled oscillators control morning and evening locomotor behaviour of Drosophila. Nature 431, 862–868 (2004).

    ADS 
    CAS 

    Google Scholar
     

  • Sheeba, V., Gu, H., Sharma, V. K., O’Dowd, D. K. & Holmes, T. C. Circadian- and light-dependent regulation of resting membrane potential and spontaneous action potential firing of Drosophila circadian pacemaker neurons. J. Neurophysiol. 99, 976–988 (2008).


    Google Scholar
     

  • Menegazzi, P. et al. A functional clock within the main morning and evening neurons of D. melanogaster is not sufficient for wild-type locomotor activity under changing day length. Front. Physiol. 11, 229 (2020).

    PubMed Central 

    Google Scholar
     

  • Hermann, C. et al. The circadian clock network in the brain of different Drosophila species. J. Comp. Neurol. 521, 367–388 (2013).

    CAS 

    Google Scholar
     

  • Park, J. H. et al. Differential regulation of circadian pacemaker output by separate clock genes in Drosophila. Proc. Natl Acad. Sci. USA 97, 3608–3613 (2000).

    ADS 
    CAS 
    PubMed Central 

    Google Scholar
     

  • Fernandez, M. P., Berni, J. & Ceriani, M. F. Circadian remodeling of neuronal circuits involved in rhythmic behavior. PLoS Biol. 6, e69 (2008).

    PubMed Central 

    Google Scholar
     

  • Herrero, A. et al. Coupling neuropeptide levels to structural plasticity in Drosophila clock neurons. Curr. Biol. 30, 3154–3166 (2020).

    CAS 

    Google Scholar
     

  • Zhang, L. et al. DN1(p) circadian neurons coordinate acute light and PDF inputs to produce robust daily behavior in Drosophila. Curr. Biol. 20, 591–599 (2010).

    CAS 
    PubMed Central 

    Google Scholar
     

  • Liang, X., Holy, T. E. & Taghert, P. H. A series of suppressive signals within the Drosophila circadian neural circuit generates sequential daily outputs. Neuron 94, 1173–1189 (2017).

    CAS 
    PubMed Central 

    Google Scholar
     

  • Ryczek, N., Lys, A. & Makalowska, I. The functional meaning of 5’UTR in protein-coding genes. Int. J. Mol. Sci. 24, 2976 (2023).

  • Bailey, T. L. & Elkan, C. Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc. Int. Conf. Intell. Syst. Mol. Biol. 2, 28–36 (1994).

    CAS 

    Google Scholar
     

  • Bergland, A. O., Tobler, R., Gonzalez, J., Schmidt, P. & Petrov, D. Secondary contact and local adaptation contribute to genome-wide patterns of clinal variation in Drosophila melanogaster. Mol. Ecol. 25, 1157–1174 (2016).

    CAS 
    PubMed Central 

    Google Scholar
     

  • Arguello, J. R., Laurent, S. & Clark, A. G. Demographic history of the human commensal Drosophila melanogaster. Genome Biol. Evol. 11, 844–854 (2019).

    PubMed Central 

    Google Scholar
     

  • Khatib, L., Subasi, B. S., Fishman, B., Kapun, M. & Tauber, E. Unveiling subtle geographical clines: phenotypic effects and dynamics of circadian clock gene polymorphisms. Biology 12, 858 (2023).

    CAS 
    PubMed Central 

    Google Scholar
     

  • Lamaze, A. et al. A natural timeless polymorphism allowing circadian clock synchronization in “white nights”. Nat. Commun. 13, 1724 (2022).

    ADS 
    CAS 
    PubMed Central 

    Google Scholar
     

  • Tauber, E. et al. Natural selection favors a newly derived timeless allele in Drosophila melanogaster. Science 316, 1895–1898 (2007).

    ADS 
    CAS 

    Google Scholar
     

  • Deppisch, P. et al. Adaptation of Drosophila melanogaster to long photoperiods of high-latitude summers is facilitated by the ls-timeless allele. J. Biol. Rhythms 37, 185–201 (2022).

    CAS 
    PubMed Central 

    Google Scholar
     

  • Schrider, D. R., Ayroles, J., Matute, D. R. & Kern, A. D. Supervised machine learning reveals introgressed loci in the genomes of Drosophila simulans and D. sechellia. PLoS Genet. 14, e1007341 (2018).

    PubMed Central 

    Google Scholar
     

  • Li, J. C. & Xu, F. Influences of light-dark shifting on the immune system, tumor growth and life span of rats, mice and fruit flies as well as on the counteraction of melatonin. Biol. Signals 6, 77–89 (1997).


    Google Scholar
     

  • Emerson, K. J., Bradshaw, W. E. & Holzapfel, C. M. Concordance of the circadian clock with the environment is necessary to maximize fitness in natural populations. Evolution 62, 979–983 (2008).

    PubMed Central 

    Google Scholar
     

  • Ducatez, S., Sol, D., Sayol, F. & Lefebvre, L. Behavioural plasticity is associated with reduced extinction risk in birds. Nat. Ecol. Evol. 4, 788–793 (2020).


    Google Scholar
     

  • Menegazzi, P. et al. Adaptation of circadian neuronal network to photoperiod in high-latitude European drosophilids. Curr. Biol. 27, 833–839 (2017).

    CAS 

    Google Scholar
     

  • Shafer, O. T. et al. Widespread receptivity to neuropeptide PDF throughout the neuronal circadian clock network of Drosophila revealed by real-time cyclic AMP imaging. Neuron 58, 223–237 (2008).

    CAS 
    PubMed Central 

    Google Scholar
     

  • York, R. A. Assessing the genetic landscape of animal behavior. Genetics 209, 223–232 (2018).

    PubMed Central 

    Google Scholar
     

  • Ding, K. et al. Imaging neuropeptide release at synapses with a genetically engineered reporter. eLife 8, e46421 (2019).

    PubMed Central 

    Google Scholar
     

  • Renn, S. C., Park, J. H., Rosbash, M., Hall, J. C. & Taghert, P. H. A pdf neuropeptide gene mutation and ablation of PDF neurons each cause severe abnormalities of behavioral circadian rhythms in Drosophila. Cell 99, 791–802 (1999).

    CAS 

    Google Scholar
     

  • Duhart, J. M. et al. Circadian structural plasticity drives remodeling of E cell output. Curr. Biol. 30, 5040–5048 (2020).

    CAS 

    Google Scholar
     

  • Shahandeh, M. P., Pischedda, A. & Turner, T. L. Male mate choice via cuticular hydrocarbon pheromones drives reproductive isolation between Drosophila species. Evolution 72, 123–135 (2018).

    CAS 

    Google Scholar
     

  • Razafimandimbison, S. G., McDowell, T. D., Halford, D. A. & Bremer, B. Origin of the pantropical and nutriceutical Morinda citrifolia L. (Rubiaceae): comments on its distribution range and circumscription. J. Biogeogr. 37, 520–529 (2010).


    Google Scholar
     

  • Cook, R. K. et al. The generation of chromosomal deletions to provide extensive coverage and subdivision of the Drosophila melanogaster genome. Genome Biol. 13, R21 (2012).

    CAS 
    PubMed Central 

    Google Scholar
     

  • Shahandeh, M. P. & Turner, T. L. The complex genetic architecture of male mate choice evolution between Drosophila species. Heredity (Edinb.) 124, 737–750 (2020).


    Google Scholar
     

  • Zhou, J., Yu, W. & Hardin, P. E. CLOCKWORK ORANGE enhances PERIOD mediated rhythms in transcriptional repression by antagonizing E-box binding by CLOCK-CYCLE. PLoS Genet. 12, e1006430 (2016).

    PubMed Central 

    Google Scholar
     

  • Chiu, J. C., Low, K. H., Pike, D. H., Yildirim, E. & Edery, I. Assaying locomotor activity to study circadian rhythms and sleep parameters in Drosophila. J. Vis. Exp. 43, 2157 (2010).

  • Geissmann, Q., Garcia Rodriguez, L., Beckwith, E. J. & Gilestro, G. F. Rethomics: an R framework to analyse high-throughput behavioural data. PLoS ONE 14, e0209331 (2019).

    CAS 
    PubMed Central 

    Google Scholar
     

  • Long, X., Colonell, J., Wong, A. M., Singer, R. H. & Lionnet, T. Quantitative mRNA imaging throughout the entire Drosophila brain. Nat. Methods 14, 703–706 (2017).

    CAS 

    Google Scholar
     

  • Yuan, Y., Padilla, M. A., Clark, D. & Yadlapalli, S. Streamlined single-molecule RNA-FISH of core clock mRNAs in clock neurons in whole mount Drosophila brains. Front. Physiol. 13, 1051544 (2022).

    PubMed Central 

    Google Scholar
     

  • Bahry, E. et al. RS-FISH: precise, interactive, fast, and scalable FISH spot detection. Nat. Methods 19, 1563–1567 (2022).

    CAS 
    PubMed Central 

    Google Scholar
     

  • Holm, S. A simple sequentially rejective multiple test procedure. Scand. J. Stat. 6, 65–70 (1979).

    MathSciNet 

    Google Scholar
     

  • Ostrovsky, A., Cachero, S. & Jefferis, G. Clonal analysis of olfaction in Drosophila: immunochemistry and imaging of fly brains. Cold Spring Harb. Protoc. 2013, 342–346 (2013).


    Google Scholar
     

  • Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012).

    CAS 

    Google Scholar
     

  • Ferreira, T. A. et al. Neuronal morphometry directly from bitmap images. Nat. Methods 11, 982–984 (2014).

    CAS 
    PubMed Central 

    Google Scholar
     

  • Bischof, J., Maeda, R. K., Hediger, M., Karch, F. & Basler, K. An optimized transgenesis system for Drosophila using germ-line-specific phiC31 integrases. Proc. Natl Acad. Sci. USA 104, 3312–3317 (2007).

    ADS 
    CAS 
    PubMed Central 

    Google Scholar
     

  • Markstein, M., Pitsouli, C., Villalta, C., Celniker, S. E. & Perrimon, N. Exploiting position effects and the gypsy retrovirus insulator to engineer precisely expressed transgenes. Nat. Genet. 40, 476–483 (2008).

    CAS 
    PubMed Central 

    Google Scholar
     

  • Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797 (2004).

    CAS 
    PubMed Central 

    Google Scholar
     

  • Procter, J. B. et al. Alignment of biological sequences with Jalview. Methods Mol. Biol. 2231, 203–224 (2021).

    CAS 
    PubMed Central 

    Google Scholar
     

  • Schliep, K. P. phangorn: Phylogenetic analysis in R. Bioinformatics 27, 592–593 (2011).

    CAS 

    Google Scholar
     

  • Therneau, T. M. & Grambsch, P. M. Modelling Survival Data: Extending the Cox Model (Springer, 2000).

  • Jezovit, J. A., Alwash, N. & Levine, J. D. Using flies to understand social networks. Front. Neural Circuits 15, 755093 (2021).

    PubMed Central 

    Google Scholar
     

  • Dukas, R. Natural history of social and sexual behavior in fruit flies. Sci. Rep. 10, 21932 (2020).

    ADS 
    CAS 
    PubMed Central 

    Google Scholar
     

  • Shahandeh, M. Data from: circadian plasticity evolves through regulatory changes in a neuropeptide gene. Dryad https://doi.org/10.5061/dryad.vq83bk42z (2024).

  • Bergland, A. O. et al. Data from: secondary contact and local adaptation contribute to genome-wide patterns of clinal variation in Drosophila melanogaster. Dryad https://doi.org/10.5061/dryad.7440s (2015).

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