Insect Circadian Rhythms Research Articles

Molecular Characterization and Expression Profiles ofCryptochromeGenes in a Long-Distance Migrant,Agrotis segetum(Lepidoptera: Noctuidae)

Cryptochromes act as photoreceptors or integral components of the circadian clock that involved in the regulation of circadian clock and regulation of migratory activity in many animals, and they may also act as magnetoreceptors that sensed the direction of the Earth’s magnetic field for the purpose of navigation during animals’ migration. Light is a major environmental signal for insect circadian rhythms, and it is also necessary for magnetic orientation. We identified the full-length cDNA encoding As-CRY1 and As-CRY2 in Agrotis segetum Denis and Schiffermaller (turnip moth (Lepidoptera: Noctuidae)). The DNA photolyase domain and flavin adenine dinucleotide-binding domain were found in both cry genes, and multiple alignments showed that those domains that are important for the circadian clock and magnetosensing were highly conserved among different animals. Quantitative polymerase chain reaction showed that cry genes were expressed in all examined body parts, with higher expression in adults during the developmental stages of the moths. Under a 14:10 (L:D) h cycle, the expression of cry genes showed a daily biological rhythm, and light can affect the expression levels of As-cry genes. The expression levels of cry genes were higher in the migratory population than in the reared population and higher in the emigration population than in the immigration population. These findings suggest that the two cryptochrome genes characterized in the turnip moth might be associated with the circadian clock and magnetosensing. Their functions deserve further study, especially for potential control of the turnip moth.

Editorial: Current Trends of Insect Physiology and Population Dynamics: Modeling Insect Phenology, Demography, and Circadian Rhythms in Variable Environments

Editorial: Current Trends of Insect Physiology and Population Dynamics: Modeling Insect Phenology, Demography, and Circadian Rhythms in Variable Environments

Time-Dependent Trapping of Pollinators Driven by the Alignment of Floral Phenology with Insect Circadian Rhythms.

Several evolutionary lineages in the early divergent angiosperm family Annonaceae possess flowers with a distinctive pollinator trapping mechanism, in which floral phenological events are very precisely timed in relation with pollinator activity patterns. This contrasts with previously described angiosperm pollinator traps, which predominantly function as pitfall traps. We assess the circadian rhythms of pollinators independently of their interactions with flowers, and correlate these data with detailed assessments of floral phenology. We reveal a close temporal alignment between patterns of pollinator activity and the floral phenology driving the trapping mechanism (termed ‘circadian trapping’ here). Non-trapping species with anthesis of standard duration (c. 48 h) cannot be pollinated effectively by pollinators with a morning-unimodal activity pattern; non-trapping species with abbreviated anthesis (23–27 h) face limitations in utilizing pollinators with a bimodal circadian activity; whereas species that trap pollinators (all with short anthesis) can utilize a broader range of potential pollinators, including those with both unimodal and bimodal circadian rhythms. In addition to broadening the range of potential pollinators based on their activity patterns, circadian trapping endows other selective advantages, including the possibility of an extended staminate phase to promote pollen deposition, and enhanced interfloral movement of pollinators. The relevance of the alignment of floral phenological changes with peaks in pollinator activity is furthermore evaluated for pitfall trap pollination systems.

Dedicated Issue ‐ Biochronometry in Insects

This issue collects papers on biochronometry, i.e., biological time measurement, in insects including circadian and non-circadian rhythms and photoperiodism. This is dedicated to Professor Sinzo Masaki to celebrate his 90th year. He has been one of the leaders in this field and served Physiological Entomology as an editorial advisor for more than 23 years (1985–2008). David Saunders and Graham Goldsworthy kindly wrote tributes to him for this issue. Time measurement has been under the spotlight in insect physiology. Major concepts in chronobiology were proposed on experimental results in insect circadian rhythms: Gate for population rhythms, temperature compensation of the period, etc. In photoperiodism, major theoretical models for measuring the day- or night-length were developed also on experimental results in insects. Moreover, biological rhythms with periods far from a day, i.e., circannual, circatidal, circa(semi)lunar rhythms, were also discovered in insects. Although most of these results were reported in the second half of the 20th century, this scientific field is still evolving with development of technology, such as cell-specific gene expression, RNAi, next generation DNA sequencing, and genome editing. This issue collects three reviews and seven original papers. The reviews deal with circadian factors in adaptation to natural or man-made environment. The original papers report recent progress in biochronometry, including sleep regulation, resetting of a circadian and a circannual clock, circadian control of metabolism, diapause induction mechanisms, and a novel approach to a photoperiodic time-measurement mechanism. Although these papers cover only a small fraction of the fields related to biochronometry in insects, we hope this issue will help to introduce readers to several new aspects of insect biochronometry and provide motivation for further research on this fascinating topic.

The nuclear receptor genes HR3 and E75 are required for the circadian rhythm in a primitive insect.

Insect circadian rhythms are generated by a circadian clock consisting of transcriptional/translational feedback loops, in which CYCLE and CLOCK are the key elements in activating the transcription of various clock genes such as timeless (tim) and period (per). Although the transcriptional regulation of Clock (Clk) has been profoundly studied, little is known about the regulation of cycle (cyc). Here, we identify the orphan nuclear receptor genes HR3 and E75, which are orthologs of mammalian clock genes, Rorα and Rev-erbα, respectively, as factors involved in the rhythmic expression of the cyc gene in a primitive insect, the firebrat Thermobia domestica. Our results show that HR3 and E75 are rhythmically expressed, and their normal, rhythmic expression is required for the persistence of locomotor rhythms. Their RNAi considerably altered the rhythmic transcription of not only cyc but also tim. Surprisingly, the RNAi of HR3 revealed the rhythmic expression of Clk, suggesting that this ancestral insect species possesses the mechanisms for rhythmic expression of both cyc and Clk genes. When either HR3 or E75 was knocked down, tim, cyc, and Clk or tim and cyc, respectively, oscillated in phase, suggesting that the two genes play an important role in the regulation of the phase relationship among the clock genes. Interestingly, HR3 and E75 were also found to be involved in the regulation of ecdysis, suggesting that they interconnect the circadian clock and developmental processes.

Effects of temperature on circadian rhythm in the Japanese honeybee, Apis cerana japonica

Temperature influences key aspects of insect circadian rhythms. The locomotor rhythm in foragers of the Japanese honeybee, Apis cerana japonica, was entrained to a skeleton temperature cycle. An initial warm temperature pulse was imposed at the beginning of subjective day and a second was applied at the end of the subjective day. A single warm pulse given every early subjective day in constant darkness (DD) entrained the locomotor rhythm without a second temperature pulse, but a single pulse given in late subjective day allowed a free-running rhythm. When honeybees were kept under a light–dark cycle, their body temperatures increased by 7–8 °C with locomotor activity. This temperature elevation remained during the photophase but followed the ambient environmental temperature at night. Body temperature oscillations continued to be circadian in DD, and temperature elevation occurred during the subjective day. In DD, the free-running period τ of locomotor activity increased when the ambient temperature increased from 27 to 37 °C, although these changes were within the range of temperature compensation for many organisms. Under continuous light conditions (LL), τ remained constant with more strict temperature compensation. Patterns of brain period mRNA levels of forager bees maintained at different temperatures in LL revealed that the free-running period of per mRNA rhythm was temperature compensated. In addition, temperature strongly influenced the amplitude of the circadian transcriptional rhythms during the free-run period in LL, which may confer temperature compensation. We also discuss the possibility that daily changes in forager body temperatures may act as an internal Zeitgeber by fluctuating hive temperature.

PACAP and PDF signaling in the regulation of mammalian and insect circadian rhythms

Endogenous circadian clocks are inherent to all living organisms. They are needed to guarantee successful life since they regulate very important biological processes such as behavior and reproduction. Secretin-like G-protein coupled receptors are very important factors in the signal transduction pathways of circadian clocks. In this review, we will focus on the role of two secretin-like signaling pathways that play an important role in the regulation of the mammalian and the insect clock, respectively: the pituitary adenylate cyclase-activating polypeptide (PACAP) and pigment dispersing factor (PDF) signaling pathways. Both pathways are most likely related although their function in the biological clock differs.

Double-labelled in situ Hybridization Reveals the Lack of Co-localization of mRNAs for the Circadian Neuropeptide PDF and FMRFamide in Brains of the Flies Musca domestica and Drosophila melanogaster

Many lines of evidence have suggested that neuropeptides other than pigment-dispersing factor (PDF) are involved in regulating insect circadian rhythms, and FMRFamide-related peptides are additional candidates acting as such neuromodulators. Double-immunolabelling in insect brains with anti-crustacean beta-PDH and anti-FMRFamide antibodies had previously suggested that insect PDF and FMRFamide-like peptides may coexist in the same cells. However, it is critical for this kind of comparative investigations to use antibodies of proven specificity, to eliminate the possibility of both reciprocal cross-reactivity and the detection of unknown peptides. In the present study, we achieved the cDNA cloning of an fmrf mRNA from the housefly Musca domestica, for which co-localization of FMRFamide and PDF peptides was previously suggested. In order to examine the possible co-expression of this gene with the pdf gene, we carried out double-labelled in situ hybridization for simultaneous detection of both pdf and fmrf mRNAs in housefly, Musca brains. The results clearly indicated that they occur in distinctly different cells. This was also proven for the fruit fly Drosophila melanogaster by similar double-labelled in situ hybridization. The results thus revealed no reason to evoke the physiological release of FMRFamide and PDF peptides from the same neurons.

Honey bee circadian clocks: behavioral control from individual workers to whole-colony rhythms

In the field of insect circadian rhythms, the honey bee is best known for its foraging time-sense, or Zeitgedächtnis, which permits the forager bee to make precise associations between the presence of food and the time of day. A number of studies, now considered classics, established that bees could be trained to collect food at virtually any time of the circadian cycle and that this timekeeping ability was controlled by an endogenous circadian clock. Recently, behavioral rhythms in bees have been examined using a variety of approaches, in both laboratory and field studies. The following areas of new research are reviewed: (a) the ontogeny of behavioral rhythmicity in newly emerged worker bees; (b) the integration of behavioral rhythmicity with the colony's division of labor; (c) the evidence for social entrainment of behavioral rhythms and for a ‘clock of the colony’; (d) the potential linkage between circadian rhythms of general locomotor activity and the foraging time-sense; (e) learning and entrainment hypotheses proposed to explain the mechanism underlying the time-sense; (f) the interplay between extinction and persistence of the time-memory as revealed from the differential behavior of individuals within the foraging group; and (g) comparisons of the Zeitgedächtnis with food-anticipatory rhythms in other animals.

An Extraretinally Expressed Insect Cryptochrome with Similarity to the Blue Light Photoreceptors of Mammals and Plants

Photic entrainment of insect circadian rhythms can occur through either extraretinal (brain) or retinal photoreceptors, which mediate sensitivity to blue light or longer wavelengths, respectively. Although visual transduction processes are well understood in the insect retina, almost nothing is known about the extraretinal blue light photoreceptor of insects. We now have identified and characterized a candidate blue light photoreceptor gene in Drosophila (DCry) that is homologous to the cryptochrome (Cry) genes of mammals and plants. The DCry gene is located in region 91F of the third chromosome, an interval that does not contain other genes required for circadian rhythmicity. The protein encoded by DCry is approximately 50% identical to the CRY1 and CRY2 proteins recently discovered in mammalian species. As expected for an extraretinal photoreceptor mediating circadian entrainment, DCry mRNA is expressed within the adult brain and can be detected within body tissues. Indeed, tissue in situ hybridization demonstrates prominent expression in cells of the lateral brain, which are close to or coincident with the Drosophila clock neurons. Interestingly, DCry mRNA abundance oscillates in a circadian manner in Drosophila head RNA extracts, and the temporal phasing of the rhythm is similar to that documented for the mouse Cry1 mRNA, which is expressed in clock tissues. Finally, we show that changes in DCry gene dosage are associated predictably with alterations of the blue light resetting response for the circadian rhythm of adult locomotor activity.

Insect circadian rhythms and photoperiodism.

Two clock-controlled processes, overt circadian rhythmicity and the photoperiodic induction of diapause, are described in the blow fly, Calliphora vicina and the fruit fly, Drosophila melanogaster. Circadian locomotor rhythms of the adult flies reflect endogenous, self-sustained oscillations with a temperature compensated period. The free-running rhythms become synchronised (entrained) to daily light:dark cycles, but become arrhythmic in constant light above a certain intensity. Some flies show fragmented rhythms (internal desynchronisation) suggesting that overt rhythmicity is the product of a multioscillator (multicellular) system. Photoperiodic induction of larval diapause in C. vicina and of ovarian diapause in D. melanogaster is also based on the circadian system but seems to involve a separate mechanism at both the molecular and neuronal levels. For both processes in both species, the compound eyes and ocelli are neither essential nor necessary for photic entrainment, and the circadian clock mechanism is not within the optic lobes. The central brain is the most likely site for both rhythm generation and extra-optic photoreception. In D. melanogaster, a group of lateral brain neurons has been identified as important circadian pacemaker cells, which are possibly also photo-sensitive. Similar lateral brain neurons, staining for arrestin, a protein in the phototransduction 'cascade' and a selective marker for photoreceptors in both vertebrates and invertebrates, have been identified in C. vicina. Much less is known about the cellular substrate of the photoperiodic mechanism, but this may involve the pars intercerebralis region of the mid-brain.

Entomology Comes Alive with Video

Insects Display many behaviors that are difficult to describe verbally or to illustrate by still or motion photography. However, understanding of these behaviors, which include molting, pupation, feeding, predation, parasitism, and locomotion, is essential for the entomology student (Borror et al. 1981, Daly et al. 1978). Many of these activities cannot be demonstrated in classroom laboratories with live specimens due to insect circadian rhythms, time limitations, and a general lack of performance and cooperation by insect subjects. Seasonal constraints can also limit the availability of live insect specimens. These problems are not limited to entomology and occur in other zoological disciplines.

Insect circadian rhythms transmitted by parabiosis--a re-examination.

FIFTEEN years of research on the hormonal control of insect circadian rhythms has been founded on the original report that rhythms could be transmitted in the blood between para-biosed cockroaches1. The interpretation of this experiment has been questioned, however, for the following reasons, (a) No control parabioses were performed using animals with unconnected haemocoels2. (b) The lower (recipient) animal was supposedly made arrhythmic by keeping it in constant light (LL), whereas it is now known that cockroaches can remain rhythmic for weeks in LL3 and that such rhythms may not necessarily be apparent in the locomotor activity4, (c) No cognizance was taken of the phase of the recipient animal, which may therefore have been close to that of the donor5. (d) The recipient animal was intact and therefore in possession of a complete neuro-endocrine system whose clock may simply have been re-started by the shock of the operation6.

How are insect circadian rhythms controlled?

A review of available evidence—mostly involving the cockroach—suggests that insect circadian rhythms are not controlled primarily by hormones. The primary pace-maker seems rather to be electrical, acting through the ventral nerve cord.

Endocrine and nervous factors in insect circadian rhythms.

Endocrine and nervous factors in insect circadian rhythms.

Modifications of Activity Rhythm of Periplaneta americana (L.), Induced by Carbon Dioxide and Nitrogen

Previous article No AccessModifications of Activity Rhythm of Periplaneta americana (L.), Induced by Carbon Dioxide and NitrogenCharles L. RalphCharles L. Ralph Search for more articles by this author PDFPDF PLUS Add to favoritesDownload CitationTrack CitationsPermissionsReprints Share onFacebookTwitterLinkedInRedditEmail SectionsMoreDetailsFiguresReferencesCited by Volume 32, Number 1Jan., 1959 Article DOIhttps://doi.org/10.1086/physzool.32.1.30152293 Views: 2Total views on this site Citations: 9Citations are reported from Crossref Journal History This article was published in Physiological Zoology (1928-1998), which is continued by Physiological and Biochemical Zoology (1999-present). Copyright 1959 The University of ChicagoPDF download Crossref reports the following articles citing this article:D. D. Branscome, P. G. Koehler, F. M. Oi Influence of carbon dioxide gas on German cockroach (Dictyoptera: Blattellidae) knockdown, recovery, movement and feeding, Physiological Entomology 30, no.22 (Jun 2005): 144–150.https://doi.org/10.1111/j.1365-3032.2005.00439.xJeffrey W Harris, Joseph Woodring, John R Harbo Effects of carbon dioxide on levels of biogenic amines in the brains of queenless worker and virgin queen honey bees ( Apis mellifera ), Journal of Apicultural Research 35, no.22 (Mar 2015): 69–78.https://doi.org/10.1080/00218839.1996.11100915J. Machin, M. J. O’donnell, P. Kestler Evidence Against Hormonal Control of Integumentary Water Loss in Periplaneta Americana, Journal of Experimental Biology 121, no.11 (Mar 1986): 339–348.https://doi.org/10.1242/jeb.121.1.339Akira Tanaka Effects of carbon-dioxide anaesthesia on the number of instars, larval duration and adult body size of the German cockroach, Blattella germanica, Journal of Insect Physiology 28, no.1010 (Jan 1982): 813–821.https://doi.org/10.1016/0022-1910(82)90092-0J.P. Woodring, C.W. Clifford, R.M. Roe, B.R. Beckman Effects of CO2 and anoxia on feeding, growth, metabolism, water balance, and blood composition in larval female house crickets, Acheta domesticus, Journal of Insect Physiology 24, no.6-76-7 (Jan 1978): 499–509.https://doi.org/10.1016/0022-1910(78)90051-3William M. Banks, Alease S. Bruce, Harold T. Peart The effects of temperature, sex and circadian rhythm on oxygen consumption in two species of cockroaches, Comparative Biochemistry and Physiology Part A: Physiology 52, no.11 (Jan 1975): 223–227.https://doi.org/10.1016/S0300-9629(75)80157-5John Brady The Physiology of Insect Circadian Rhythms, (Jan 1974): 1–115.https://doi.org/10.1016/S0065-2806(08)60129-0Robert B. Suter, Kenneth S. Rawson Circadian Activity Rhythm of the Deer Mouse, Peromyscus : Effect of Deuterium Oxide, Science 160, no.38313831 (May 1968): 1011–1014.https://doi.org/10.1126/science.160.3831.1011R. De G. Weevers A Lepidopteran Saline: Effects of Inorganic Cation Concentrations On Sensory, Reflex and Motor Responses in A Herbivorous Insect, Journal of Experimental Biology 44, no.11 (Feb 1966): 163–175.https://doi.org/10.1242/jeb.44.1.163