Circadian clocks are synchronized with the external environment by light and temperature. The effect of these cues on behavior is well-characterized in Drosophila, however, little is known about synchronization in non-model insect species. Therefore, we explored entrainment of locomotor activity by light and temperature in the linden bug Pyrrhocoris apterus (Heteroptera), an insect species with a strong seasonal response (reproductive diapause), which is triggered by both photoperiod and thermoperiod. Our results show that either light or temperature cycles are strong factors entraining P. apterus locomotor activity. Pyrrhocoris is able to be partially synchronized by cycles with temperature amplitude as small as 3°C and more than 50% of bugs is synchronized by 5°C steps. If conflicting zeitgebers are provided, light is the stronger signal. Linden bugs lack light-sensitive (Drosophila-like) cryptochrome. Notably, a high percentage of bugs is rhythmic even in constant light (LL) at intensity ∼400 lux, a condition which induces 100% arrhythmicity in Drosophila. However, the rhythmicity of bugs is still reduced in LL conditions, whereas rhythmicity remains unaffected in constant dark (DD). Interestingly, a similar phenomenon is observed after temperature cycles entrainment. Bugs released to constant thermophase and DD display weak rhythmicity, whereas strong rhythmicity is observed in bugs released to constant cryophase and DD. Our study describes the daily and circadian behavior of the linden bug as a response to photoperiodic and thermoperiodic entraining cues. Although the molecular mechanism of the circadian clock entrainment in the linden bug is virtually unknown, our study contributes to the knowledge of the insect circadian clock features beyond Drosophila research.

Faculty of Science University of South Bohemia České Budějovice Czechia

Institute of Entomology Biology Centre of Academy of Sciences of the Czech Republic České Budějovice Czechia

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Aschoff J. (1984). Circadian timing. PubMed DOI

Bajgar A., Dolezel D., Hodkova M. (2013a). Endocrine regulation of non-circadian behavior of circadian genes in insect gut. PubMed DOI

Bajgar A., Jindra M., Dolezel D. (2013b). Autonomous regulation of the insect gut by circadian genes acting downstream of juvenile hormone signaling. PubMed DOI PMC

Bazalova O., Dolezel D. (2017). Daily activity of the housefly, PubMed DOI PMC

Boothroyd C. E., Wijnen H., Naef F., Saez L., Young M. W. (2007). Integration of light and temperature in the regulation of circadian gene expression in PubMed DOI PMC

Brown L. A., Fisk A. S., Pothecary C. A., Peirson S. N. (2019). Telling the time with a broken clock: quantifying circadian disruption in animal models. PubMed DOI PMC

Currie J., Goda T., Wijnen H. (2009). Selective entrainment of the PubMed DOI PMC

Ditrich T., Janda V., Vaneckova H., Dolezel D. (2018). Climatic variation of supercooling point in the the linden bug PubMed DOI PMC

Dolezel D., Sauman I., Kost’al V., Hodkova M. (2007). Photoperiodic and food signals control expression pattern of the clock gene, period, in the linden bug, PubMed DOI

Dolezelova E., Dolezel D., Hall J. C. (2007). Rhythm defects caused by newly engineered null mutations in PubMed DOI PMC

Dunlap J. C., Loros J. J., DeCoursey P. J. (2004).

Emery P., Stanewsky R., Helfrich-Forster C., Emery-Le M., Hall J. C., Rosbash M. (2000). PubMed DOI

Glaser F. T., Stanewsky R. (2005). Temperature synchronization of the PubMed DOI

Hamblen M. J., White N. E., Emery P., Kaiser K., Hall J. C. (1998). Molecular and behavioral analysis of four period mutants in PubMed PMC

Hardin P. E. (2011). Molecular genetic analysis of circadian timekeeping in PubMed DOI PMC

Harper R. E., Dayan P., Albert J. T., Stanewsky R. (2016). Sensory conflict disrupts activity of the PubMed DOI PMC

Helfrich-Förster C. (2019). Light input pathways to the circadian clock of insects with an emphasis on the fruit fly PubMed PMC

Hodkova M. (1976). Nervous inhibition of corpora allata by photoperoid in PubMed DOI

Hodkova M., Syrova Z., Dolezel D., Sauman I. (2003). DOI

Kannan N. N., Tomiyama Y., Nose M., Tokuoka A., Tomioka K. (2019). Temperature entrainment of circadian locomotor and transcriptional rhythms in the cricket, PubMed DOI

Komada S., Kamae Y., Koyanagi M., Tatewaki K., Hassaneen E., Saifullah A., et al. (2015). Green-sensitive opsin is the photoreceptor for photic entrainment of an insect circadian clock. PubMed DOI PMC

Kostal V., Tollarova M., Dolezel D. (2008). Dynamism in physiology and gene transcription during reproductive diapause in a heteropteran bug, PubMed DOI

Kotwica-Rolinska J., Chodakova L., Chvalova D., Kristofova L., Fenclova I., Provaznik J., et al. (2019). CRISPR/Cas9 genome editing introduction and optimization in the non-model insect PubMed DOI PMC

Kotwica-Rolinska J., Pivarciova L., Vaneckova H., Dolezel D. (2017). The role of circadian clock genes in the photoperiodic timer of the linden bug, DOI

Kume K., Zylka M. J., Sriram S., Shearman L. P., Weaver D. R., Jin X., et al. (1999). mCRY1 and mCRY2 are essential components of the negative limb of the circadian clock feedback loop. PubMed DOI

Levine J. D., Funes P., Dowse H. B., Hall J. C. (2002). Resetting the circadian clock by social experience in PubMed DOI

Maguire S. E., Sehgal A. (2015). Heating and cooling the PubMed DOI PMC

Majercak J., Sidote D., Hardin P. E., Edery I. (1999). How a circadian clock adapts to seasonal decreases in temperature and day length. PubMed DOI

Matsumoto A., Tomioka K., Chiba Y., Tanimura T. (1999). timrit lengthens circadian period in a temperature-dependent manner through suppression of PERIOD protein cycling and nuclear localization. PubMed DOI PMC

Menegazzi P., Yoshii T., Helfrich-Forster C. (2012). Laboratory versus nature: the two sides of the PubMed DOI

Miyasako Y., Umezaki Y., Tomioka K. (2007). Separate sets of cerebral clock neurons are responsible for light and temperature entrainment of PubMed DOI

Moore D., Rankin M. N. (1993). Light and temperature entrainment of a locomotor rhythm in honeybees. DOI

Numata H., Saulich A. H., Volkovich T. A. (1993). Photoperiodic responses of the linden bug,

Ozkaya O., Rosato E. (2012). The circadian clock of the fly: a neurogenetics journey through time. PubMed DOI

Pittendrigh C. S. (1960). Circadian rhythms and the circadian organization of living systems. PubMed DOI

Pivarciova L., Vaneckova H., Provaznik J., Wu B. C., Pivarci M., Peckova O., et al. (2016). Unexpected geographic variability of the free running period in the linden bug, PubMed DOI

Refinetti R., Lissen G. C., Halberg F. (2007). Procedures for numerical analysis of circadian rhythms. PubMed DOI PMC

Roessingh S., Rosing M., Marunova M., Ogueta M., George R., Lamaze A., et al. (2019). Temperature synchronization of the PubMed DOI PMC

Rothenfluh A., Abodeely M., Price J. L., Young M. W. (2000). Isolation and analysis of six timeless alleles that cause short- or long-period circadian rhythms in PubMed PMC

Saunders D. S. (1983). A diapause induction termination asymmetry in the photoperiodic responses of the linden bug, DOI

Saunders D. S. (1987). Insect photoperiodism: the linden bug, DOI

Saunders D. S. (1997). Insect circadian rhythms and photoperiodism. PubMed DOI

Schmid B., Helfrich-Forster C., Yoshii T. (2011). A new imageJ plug-in “ActogramJ” for chronobiological analyses. PubMed DOI

Sharma V. K., Chandrashekaran M. K. (2005). Zeitgebers (time cues) for biological clocks.

Shaw B., Fountain M., Wijnen H. (2019). Control of daily locomotor activity patterns in PubMed DOI

Singh S., Giesecke A., Damulewicz M., Fexová S., Mazzotta G. M., Stanewsky R., et al. (2019). New PubMed DOI PMC

Smykal V., Bajgar A., Provaznik J., Fexova S., Buricova M., Takaki K., et al. (2014). Juvenile hormone signaling during reproduction and development of the linden bug, PubMed DOI

Stanewsky R., Kaneko M., Emery P., Beretta B., Wager-Smith K., Kay S. A., et al. (1998). The PubMed DOI

Tataroglu O., Emery P. (2015). The molecular ticks of the PubMed DOI PMC

Tokuoka A., Itoh T. Q., Hori S., Uryu O., Danbara Y., Nose M., et al. (2017). cryptochrome genes form an oscillatory loop independent of the PubMed DOI PMC

Tomioka K., Matsumoto A. (2010). A comparative view of insect circadian clock systems. PubMed DOI PMC

Tomioka K., Yoshii T. (2006). Entrainment of DOI

Urbanova V., Bazalova O., Vaneckova H., Dolezel D. (2016). Photoperiod regulates growth of male accessory glands through juvenile hormone signaling in the linden bug, PubMed DOI

Vanin S., Bhutani S., Montelli S., Menegazzi P., Green E. W., Pegoraro M., et al. (2012). Unexpected features of PubMed DOI

Wheeler D. A., Hamblencoyle M. J., Dushay M. S., Hall J. C. (1993). Behavior in light dark cycles of PubMed DOI

Wolfgang W., Simoni A., Gentile C., Stanewsky R. (2013). The Pyrexia transient receptor potential channel mediates circadian clock synchronization to low temperature cycles in PubMed DOI PMC

Yoshii T., Fujii K., Tomioka K. (2007). Induction of PubMed DOI

Yoshii T., Hermann C., Helfrich-Forster C. (2010). Cryptochrome-positive and -negative clock neurons in PubMed DOI

Yoshii T., Sakamoto M., Tomioka K. (2002). A temperature-dependent timing mechanism is involved in the circadian system that drives locomotor rhythms in the fruit fly PubMed DOI

Yuan Q., Metterville D., Briscoe A. D., Reppert S. M. (2007). Insect cryptochromes: gene duplication and loss define diverse ways to construct insect circadian clocks. PubMed DOI

Zielinski T., Moore A. M., Troup E., Halliday K. J., Millar A. J. (2014). Strengths and limitations of period estimation methods for circadian data. PubMed DOI PMC

Coevolution of Drosophila-type timeless with partner clock proteins

Impact of photoperiod and functional clock on male diapause in cryptochrome and pdf mutants in the linden bug Pyrrhocoris apterus

Pigment Dispersing Factor Is a Circadian Clock Output and Regulates Photoperiodic Response in the Linden Bug, Pyrrhocoris apterus

Loss of Timeless Underlies an Evolutionary Transition within the Circadian Clock

Functional analysis and localisation of a thyrotropin-releasing hormone-type neuropeptide (EFLa) in hemipteran insects