SEARCH

SEARCH BY CITATION

Keywords:

  • Clock models;
  • insect photoperiodism;
  • photoreceptors;
  • spectral sensitivity

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Models for the insect photoperiodic ‘clock’
  5. Photoreceptors at the organ level
  6. Spectral sensitivity of the photoperiodic response
  7. Photoreception in the parasitic wasp N. vitripennis
  8. Photoreception in the green vetch aphid M. viciae
  9. Photoreception in flesh flies (Sarcophaga spp.)
  10. What are the photopigments involved in insect photoperiodism?
  11. The evolution of photoperiodic clocks in insects and mites and their photoreceptive inputs
  12. Summary
  13. Acknowledgements
  14. References

This review examines the spectral sensitivities of photoperiodic responses in insects and mites in relation to circadian-based models for the photoperiodic clock. It concludes that there are probably a number of different photoreceptors at both the organ and molecular levels. These latter probably fall into two classes: (i) a blue-light sensitive photoreceptor and (ii) a range of opsins (i.e. opsin proteins conjugated with a vitamin A based pigment) absorbing light at a range of wavelengths. In flesh flies (Sarcophaga spp. and possibly other higher Diptera), which are considered to exemplify the ‘external coincidence’ model, entrainment of the photoperiodic oscillator probably involves a blue-light photoreceptor of Drosophila-type CRYPTOCHROME (CRY1) absorbing maximally at approximately 470 nm, whereas opsins absorbing at longer wavelengths may be involved in the photo-inductive process (diapause/nondiapause regulation) that occurs when dawn light coincides with the photo-inducible phase. In the parasitic wasp Nasonia vitripennis, on the other hand, a species that lacks CRY1 but expresses the nonphotosensitive ‘mammalian-type’ CRY2, and is considered to exemplify ‘internal coincidence’, entrainment of the dawn and dusk oscillators may involve opsin-based photoreceptors absorbing light at longer wavelengths as far as the red end of the spectrum. In the Lepidoptera, which express both CRY1 and CRY2, properties of both external and internal coincidence may be evident. The presence or absence of cry1 in the genome may thus emerge as a key to the photoperiodic mechanism on its light input pathway.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Models for the insect photoperiodic ‘clock’
  5. Photoreceptors at the organ level
  6. Spectral sensitivity of the photoperiodic response
  7. Photoreception in the parasitic wasp N. vitripennis
  8. Photoreception in the green vetch aphid M. viciae
  9. Photoreception in flesh flies (Sarcophaga spp.)
  10. What are the photopigments involved in insect photoperiodism?
  11. The evolution of photoperiodic clocks in insects and mites and their photoreceptive inputs
  12. Summary
  13. Acknowledgements
  14. References

Seasonal changes are characteristic of the Earth's climate, particularly at higher latitudes where ‘favourable’ summers alternate with winters that are largely inimical to an organism's growth, development or reproduction. In response to such seasonality, insects, similar to many other organisms, from fungi (Roenneberg et al., 2010) to mammals (Kriegsfeld & Bittman, 2010), have evolved mechanisms to counteract or synchronize with these events by using photoperiodic ‘clocks’ to measure and respond to changes in day length or (more usually) to night length (Saunders, 2002).

In many insects, the main response to lengthening autumnal nights is the induction of a dormant or diapause state (Saunders, 2002; Nishizuka et al., 1998; Koštál, 2011; Saunders & Bertossa, 2011), which may occur at different, although usually species-specific, stages of development, from the egg (embryo) through larva and pupa to the adult instar. In others, such as aphids, photoperiod regulates the production of seasonal morphs, with short nights of summer inducing parthenogenetic virginoparae, whereas the long nights of autumn lead to the production of sexual forms (oviparae), which in turn may lay diapausing eggs (Hardie, 2010). This review examines the light signals important in the regulation of diapause and seasonal morphs, in relation to various models for the photoperiodic mechanism and the nature of the photoreceptors involved.

Models for the insect photoperiodic ‘clock’

  1. Top of page
  2. Abstract
  3. Introduction
  4. Models for the insect photoperiodic ‘clock’
  5. Photoreceptors at the organ level
  6. Spectral sensitivity of the photoperiodic response
  7. Photoreception in the parasitic wasp N. vitripennis
  8. Photoreception in the green vetch aphid M. viciae
  9. Photoreception in flesh flies (Sarcophaga spp.)
  10. What are the photopigments involved in insect photoperiodism?
  11. The evolution of photoperiodic clocks in insects and mites and their photoreceptive inputs
  12. Summary
  13. Acknowledgements
  14. References

Photoperiodic responses have evolved on many occasions as insects extended their distributions into higher latitudes with a pronounced winter. Accumulating evidence strongly suggests that most (perhaps all) photoperiodic mechanisms are based on the pre-existing circadian system, an idea first proposed some 75 years ago by the German plant physiologist Erwin Bünning (Bünning, 1936). In probably all cases, the evolved mechanisms used circadian oscillations as ‘the clock’ (Saunders, 2011), although these now show differences in detail that reflect differences in their underlying molecular architecture.

Circadian-based models for the insect photoperiodic mechanism have been reviewed on a number of occasions (Vaz Nunes & Saunders, 1999; Saunders, 2002, 2011). For example, based on numerous formal studies of circadian rhythmicity, Pittendrigh (1972) suggests several theoretical possibilities for photoperiodic induction based upon Bünning's general hypothesis. These include, amongst others, the models ‘internal coincidence’ and ‘external coincidence’. In brief, the internal coincidence model suggests that two separate ‘dawn’ and ‘dusk’ (morning and evening) oscillators are involved, with seasonal changes in photoperiod being measured as differences in the phase relationships between the two as day length or night length changed. In this model, light may have a single role (i.e. that of entrainment). By contrast, external coincidence (Pittendrigh & Minis, 1964; Pittendrigh, 1966) consists of a single oscillator entrained by the light/dark cycle in such a way that a particular light-sensitive phase (termed the photo-inducible phase, ϕi) falls in the latter half of the night. In the long nights of autumn, ϕifalls in the dark, leading to the induction of diapause (or an autumnal morph), whereas, in the short nights of summer, the dawn transition of the photophase extends ‘backwards’ to illuminate ϕI, thus inducing continuous or nondiapause development. In this model, light has two roles: ‘entrainment’ of the circadian oscillation(s) to the light cycle and ‘photoregulation’ of the alternate nondiapause or diapause pathways by illumination or non-illumination of the photo-inducible phase.

Details of these and other models have been reviewed previously (Vaz Nunes & Saunders, 1999; Saunders, 2011), together with experimental evidence and tests to discriminate between them, particularly for the parasitic wasp Nasonia vitripennis and the flesh fly Sarcophaga argyrostoma, which are species considered to present features of internal and external coincidence, respectively.

Photoreceptors at the organ level

  1. Top of page
  2. Abstract
  3. Introduction
  4. Models for the insect photoperiodic ‘clock’
  5. Photoreceptors at the organ level
  6. Spectral sensitivity of the photoperiodic response
  7. Photoreception in the parasitic wasp N. vitripennis
  8. Photoreception in the green vetch aphid M. viciae
  9. Photoreception in flesh flies (Sarcophaga spp.)
  10. What are the photopigments involved in insect photoperiodism?
  11. The evolution of photoperiodic clocks in insects and mites and their photoreceptive inputs
  12. Summary
  13. Acknowledgements
  14. References

Entrainment of the circadian activity rhythm in Drosophila melanogaster involves a number of photoreceptors and photopigments, including cryptochrome, compound eyes, ocelli, Hofbauer-Buchner eyelets and unknown photopigments in the clock-gene expressing dorsal neurones (Rieger et al., 2003). A similar multiplicity of photoreceptors and photopigments is probably to be expected in insect photoperiodism, both within and between particular species.

Early observations, particularly with larvae and pupae of Lepidoptera, suggest that photoperiodic reception was a function of the brain. For example, Williams (1963) and Williams & Adkisson (1964) transplanted brains of diapausing pupae of the silkmoth Antheraea pernyi, from the head to the abdomen, and demonstrated that termination of pupal diapause by long days was transplanted along with the brain. A similar result was obtained by Claret (1966) for larvae of the large cabbage white butterfly Pieris brassicae. A clearer demonstration that the brain contained photoperiodic receptors was later provided by Bowen et al. (1984) who excised brain-retrocerebral complexes from diapause-destined larvae of the hawk moth Manduca sexta and exposed them in vitro to three long-day cycles before transplanting them into the abdomens of larvae committed for pupal diapause. The otherwise diapause-destined larvae were then found to reprogramme their development along a nondiapause pathway. These experiments were the first to demonstrate in vitro operation of a photoperiodic clock in any animal. They were followed by similar experiments with the silk moth Bombyx mori (Hasegawa & Shimizu, 1987).

Although the examples given above are for immature stages of Holometabola, brain photoreception also occurs in adult insects with functional compound eyes. Notable examples include the aphid Megoura viciae (Lees, 1964) and the blow fly Calliphora vicina (Saunders & Cymborowski, 1996). In the aphid, a 2-h supplementary period of illumination was transmitted through micro-illuminators to augment a short-day (ovipara-producing) photoperiod. Long-day responses (virginopara production) were then recorded after illumination of the dorsal midline of the head (directly over the brain) but less so when the light beam was directed into the compound eyes. Working with C. vicina, the brain was effectively disconnected from the compound eyes using a surgical technique to remove both optic lobes. Such flies were found to be effectively blind, although their locomotor activity rhythms were still able to entrain to a light cycle (Cymborowski et al., 1994) and lobectomized flies were still able to distinguish short from long photoperiods in the production of diapausing or nondiapausing larval progeny (Saunders & Cymborowski, 1996). These studies suggested that the brain was sufficient for photoreception, although the compound eyes could also play a role in intact flies.

The first evidence that compound eyes acted as photoperiodic photoreceptors comes from studies with the beetle Pterostichus nigrita (Ferenz, 1975), in which bilateral extirpation of the eyes in male beetles leads to suppressed maturation of the sperm, as if in continuous darkness. In the bean bug Riptortus pedestris, a variety of techniques, including eye ablation, are shown to block ovarian diapause regulation (Numata & Hidaka, 1983). In subsequent studies, which were conducted to a large extent by Hideharu Numata and colleagues (Goto et al. (2010)), diapause regulation in a number of other Heteroptera and Orthoptera is shown to involve the compound eyes as the principal, if not the only, photoperiodic photoreceptors. However, a possible role for the brain is suggested for the heteropteran Plautia stali (Morita & Numata, 1999). In the beetle Leptocarabus kumagaii, compound eyes are shown to be the receptors in the adults, although stemmata are found to be important in the larvae (Shintani & Numata, 2009). Lastly, in the black blow fly Protophormia terraenovae, ovarian diapause is shown to be regulated by light perceived by the compound eyes (Shiga & Numata, 1997), a situation differing from that in the related blow fly C. vicina (Saunders & Cymborowski, 1996) in which the brain appears to be the principal photoreceptor. In conclusion, several different photoperiodic photoreceptors, both between and within particular species, may be observed in the insects, including the brain, compound eyes and larval stemmata. There is, however, no evidence at present for such a role for the ocelli.

Spectral sensitivity of the photoperiodic response

  1. Top of page
  2. Abstract
  3. Introduction
  4. Models for the insect photoperiodic ‘clock’
  5. Photoreceptors at the organ level
  6. Spectral sensitivity of the photoperiodic response
  7. Photoreception in the parasitic wasp N. vitripennis
  8. Photoreception in the green vetch aphid M. viciae
  9. Photoreception in flesh flies (Sarcophaga spp.)
  10. What are the photopigments involved in insect photoperiodism?
  11. The evolution of photoperiodic clocks in insects and mites and their photoreceptive inputs
  12. Summary
  13. Acknowledgements
  14. References

Table 1 lists examples of insects and mites whose photoperiodic responses, including diapause induction, diapause termination and seasonal morph regulation, have been examined for their spectral sensitivity. Because the experimental methods used are variable, and no clear phylogenetic relationships have emerged from these studies, examples are arranged in an approximately chronological order that reflects the development of ideas and models.

Table 1.  Spectral sensitivity of the photoperiodic response.
SpeciesOrderMost effective wavelength (nm)Not effective (nm)Reference
Maximum sensitivity in the blue–green
Bombyx mori Lepidoptera350–510Not 610+ Kogure (1933) and
Grapholitha molesta Lepidoptera430–580Not 660+ Dickson (1949)
Panonychus ulmi Acarina365–540Not 540+ Lees (1953) and
Dendrolimus pini Lepidoptera407–530Not 585, 655 Geispitz (1957)
Pieris brassicae Lepidoptera530Not 655 Geispitz (1957) and
  400–520  Claret (1972)
Euscelis plebejus Homoptera365–550Not 600+ Müller (1964),
Antheraea pernyi Lepidoptera398–508Not 580+ Williams et al. (1965) and
Adoxophyes orana Lepidoptera460–480  Berlinger & Ankersmit (1976)
Carpocapsa pomonella Lepidoptera400–550  Norris et al. (1969)
Ostrinia nubilalis LepidopteraBlue  Gelman & Hayes (1980)
Megoura viciae a Homoptera450–470 * Lees (1971, 1981)
Aleyrodes proletella a Homoptera410–430  Adams (1986)
Chaoborus americanus a Diptera540  Bradshaw (1972)
Wyeomyia smithii a Diptera390–450  Bradshaw & Phillips (1980)
Sarcophaga crassipalpis Diptera390–540Not 550+ Gnagey & Denlinger (1984)
Sarcophaga similis a Diptera395–470 * Goto & Numata (2009)
Tetranychus urticae Acarina475–572Not 658 Suzuki et al. (2008)
SpeciesOrderEffective wavelength (nm)Reference
  1. aAction spectra performed.

  2. *Further details are provided in the text.

Sensitivity extending into longer wavelengths
Acronycta rumicis Lepidoptera407–655 Geispitz (1957)
Leptinitarsa decemlineata Coleoptera423–675 De Wilde & Bonga (1958)
Anthonomis grandis Coleoptera463–600 Harris et al. (1969)
Pectinophora gossypiella Lepidoptera480–600 Pittendrigh et al. (1970)
Nasonia vitripennis a Hymenoptera554–640* Saunders (1975a)
Pimpla instigator Hymenoptera380–700 Claret (1982)

The earliest studies frequently employed either filtered light as the ‘main’ photophase coupled with darkness (Dickson, 1949) or a ‘short’ white light photophase coupled with monochromatic light to replace the night (Geispitz, 1957). Later approaches used a short white light photophase supplemented by a few hours of monochromatic light after dusk (Bünning & Joerrens, 1960; Berlinger & Ankersmit, 1976), with the rationale being that, if the insect perceived the additional monochromatic light, the response would be altered from a short- to a long-day response. Improved protocols were then introduced using supplementary monochromatic light both before and after the white light photophase, which sometimes revealed differences between dawn and dusk photoreception (Bradshaw, 1972; Saunders, 1975a; Bradshaw & Phillips, 1980) or short monochromatic light pulses positioned either early or late in an otherwise inductive long night used to test particular models for the photoperiodic clock (Lees, 1971, 1981; Adams, 1986; Goto & Numata, 2009). Finally, and most importantly, energy-compensated action spectra have been conducted in at least six species, including the green vetch aphid M. viciae (Lees, 1981), the mosquitoes Chaoborus americana and Wyeomyia smithii (Bradshaw, 1972; Bradshaw & Phillips, 1980), the parasitic wasp N. vitripennis (Saunders, 1975a), the homopteran whitefly Aleyrodes proletella (Adams, 1986) and the flesh fly Sarcophaga similis (Goto & Numata, 2009). These studies pinpointed more accurately peaks of sensitivity, suggesting the absorption maxima of putative photoreceptors.

Generalizations from these studies are hard to find, mainly because of the variety of phenomena studied and differences in experimental design. Nevertheless, Table 1 suggests that maximum sensitivity is frequently in the blue or the blue–green region of the spectrum (400–550 nm), although some species may respond to shorter wavelengths into the ultraviolet (UV). A somewhat arbitrary distinction may also be made between those species that absorb maximally in the blue–green and those that also respond to longer wavelengths, particularly to light at the red end of the spectrum (over approximately 600 nm). Therefore, within the obvious limitations afforded by the widely different experimental protocols, the available data suggest that insects and mites may use a number of different photoperiodic light receptors, and some species may use more than one.

Further consideration of the spectral sensitivity of insect photoperiodic mechanisms will concentrate on those species for which action spectra have been determined, particularly in three well-studied examples: the parasitic wasp Nasonia vitripennis, the green vetch aphid M. viciae and flesh flies (Sarcophaga spp.).

Photoreception in the parasitic wasp N. vitripennis

  1. Top of page
  2. Abstract
  3. Introduction
  4. Models for the insect photoperiodic ‘clock’
  5. Photoreceptors at the organ level
  6. Spectral sensitivity of the photoperiodic response
  7. Photoreception in the parasitic wasp N. vitripennis
  8. Photoreception in the green vetch aphid M. viciae
  9. Photoreception in flesh flies (Sarcophaga spp.)
  10. What are the photopigments involved in insect photoperiodism?
  11. The evolution of photoperiodic clocks in insects and mites and their photoreceptive inputs
  12. Summary
  13. Acknowledgements
  14. References

Diapause induction in the parasitic wasp N. vitripennis is maternal in origin. Adult females exposed to the long days (short nights) of summer lay eggs that give rise to nondiapausing progeny, whereas those exposed to the lengthening nights of autumn produce offspring that enter diapause in their last (fourth) larval instar (Saunders, 1966).

Experimental evidence consistent with internal coincidence in the photoperiodic mechanism of N. vitripennis was provided by a series of Nanda-Hamner or ‘resonance’ experiments (Nanda & Hamner, 1958) in which adult wasps are exposed to a range of extended cycles containing different but constant white light photophases ranging in length from 4 to 28 h (Saunders, 1974). In experiments of this type, each photophase is coupled, in different experimental subsets, with periods of darkness, ranging from 8 to 72 h, to give overall light/dark cycles covering several multiples of the supposed circadian period (Fig. 1A). In N. vitripennis, such procedures reveal successive peaks and troughs of diapause incidence, approximately 24 h apart, providing evidence for the circadian basis of photoperiodic induction (Fig. 1B, C). They also show that the peaks of high diapause incidence become narrower as the duration of the photophase increases, with the ascending slopes of the peaks being parallel to dusk and the descending slopes parallel to dawn. Such a result is suggestive of a circadian-based induction mechanism comprising separate dawn and dusk oscillators, such as internal coincidence (Saunders, 1974).

image

Figure 1. The Nanda-Hamner protocol (Nanda & Hamner, 1958) as applied to the parasitic wasp Nasonia vitripennis. (A) Groups of insects are exposed, during their photoperiodic ‘sensitive period’, to repeated light/dark cycles comprising a short photophase (12 h in this example) coupled, in different experimental sub-sets, to a variable dark period to give overall cycle length up to 72 h or more. (B) Results of Nanda-Hamner experiments with N. vitripennis, showing peaks and troughs of diapause incidence at approximately 24-h intervals as the cycle length is increased (Saunders, 1974) (for further details, see text). (C) Data from these experiments redrawn as a ‘circadian topography’ to show relationships of the ascending and descending slopes of the high diapause peaks (a, b, c and d) to dusk and dawn, respectively (Saunders, 1974). These results are interpreted as evidence for ‘internal coincidence’ in the photoperiodic clock with separate ‘dawn’ and ‘dusk’ oscillators.

Download figure to PowerPoint

Tests to distinguish internal coincidence (in N. vitripennis) from external coincidence (see below) have included the substitution of thermoperiod for photoperiod (Saunders, 1973, 2011). The rationale behind this approach is two-fold: first, that thermoperiod is a recognized circadian-entraining agent and, second, that light (or temperature) has the single role of entraining the dawn and dusk oscillators in internal coincidence but no absolutely necessary photo-inductive role as in external coincidence (Pittendrigh, 1972). In this test, wasps are raised in complete darkness until the adult instar, and the adults are then exposed to square-wave temperature cycles (thermophase of 23 °C: cryophase of 13 °C), again in complete darkness. Their progeny are then examined for diapause incidence as fourth-instar larvae. The results obtained show that thermophases of less than 12 h per day are diapause inductive, whereas longer thermophases lead to the induction of continuously-developing or nondiapause larvae. A well-marked critical thermophase occurs between 12 and 14 h. In N. vitripennis, therefore, the diapause/nondiapause switch in development could be regulated by thermoperiod in the complete absence of light (as well as by photoperiod), which is a prediction consistent with the internal coincidence model (Saunders, 1973, 2011).

Action spectra for the photoperiodic induction of diapause/nondiapause larvae of N. vitripennis are obtained by exposing adult wasps to 24-h cycles consisting of 13 h of ‘white’ light augmented by 3 h of monochromatic light of varying intensity, positioned either before or after the main white light period, corresponding to the ‘dawn’ or ‘dusk’ transitions, respectively (Saunders, 1975a). The intensity of the monochromatic light is adjusted systematically until the proportion of diapausing larvae produced is approximately 50%. The rationale behind this approach is that, if the wasps respond to the additional monochromatic light, they would perceive a long day of 16 h and produce nondiapausing larvae accordingly.

The results obtained show that wasps are maximally sensitive to light in the range 554–586 nm, although with considerable sensitivity extending into the red at 617 nm or more. The insects show a somewhat reduced sensitivity to 653 nm but fail to respond to 765 nm. Sensitivity to 586 nm at the dawn transition is approximately 20-fold greater than that at dusk; otherwise, the two action spectra are very similar. There is also considerable sensitivity to light at shorter wavelengths (400–500 nm), with the rather broad action spectrum possibly indicating that more than one photoreceptor is involved.

Long wavelength sensitivity of the photoperiodic mechanism in N. vitripennis is also demonstrated in 24-h photoperiods and resonance experiments using cycles of red light (R > 600 nm) and darkness (D) (Saunders, 1974). For example, wasps exposed to cycles of RD 12 : 12 h produce almost 90% of their offspring as diapausing larvae, whereas those exposed to RD 18 : 6 h produce less than 2%. Results for the white light controls are 100% diapause under LD 12 : 12 h and 0% diapause under LD 18 : 6 h. Resonance or Nanda-Hamner experiments using 12-h pulses of red light (>600 nm) coupled with a variable number of hours of darkness, giving cycle lengths (T) up to 68 h, show that the proportion of females producing diapausing larvae is a rhythmic function of T. Up to T = 48 h, the results for red light cycles are similar to those for white. Thereafter, the red light curve is approximately 4 h in advance of that for white light, possibly suggesting that the circadian periods of component oscillators are shorter in red light cycles.

These results demonstrate unequivocally that N. vitripennis responds to wavelengths in excess of 600 nm not only for the discrimination of long from short days by the photoperiodic mechanism, but also for the entrainment of the circadian oscillators so involved.

Photoreception in the green vetch aphid M. viciae

  1. Top of page
  2. Abstract
  3. Introduction
  4. Models for the insect photoperiodic ‘clock’
  5. Photoreceptors at the organ level
  6. Spectral sensitivity of the photoperiodic response
  7. Photoreception in the parasitic wasp N. vitripennis
  8. Photoreception in the green vetch aphid M. viciae
  9. Photoreception in flesh flies (Sarcophaga spp.)
  10. What are the photopigments involved in insect photoperiodism?
  11. The evolution of photoperiodic clocks in insects and mites and their photoreceptive inputs
  12. Summary
  13. Acknowledgements
  14. References

Under the long days (short nights) of summer, the vetch aphid M. viciae produces successive generations of wingless, parthenogenetic virginoparae. When night lengths in late summer exceed approximately 9.5 h, oviparae are produced that lay over-wintering eggs. Extensive investigations by Lees (1973) suggest that this response is regulated by a non-oscillatory (i.e. noncircadian) hourglass-like mechanism commencing at dusk and ‘measuring’ the length of the night. The strongest evidence for this conclusion is the absence of peaks and troughs of long night effect in Nanda-Hamner (resonance) experiments over a range of temperatures (Lees, 1986).

An important experimental protocol used in the analysis of photoperiodic timing is the ‘night interruption’ experiment in which a diapause inductive long night is systematically interrupted by a short (i.e. 1 h) scanning pulse. Experiments of this type frequently reveal two positions in the night where such a pulse produces long-day effects; the first (point A) early in the night, and the second (point B) late in the night (Saunders, 2002).

Lees (1973) explains this bimodal response in M. viciae in terms of a linear, or noncircadian, night-length timer. His investigation included an important and elegant experiment, hereafter referred to as the ‘Lees experiment'. This experiment (illustrated in Fig. 2 for S. argyrostoma) is conducted in two halves. In the first half (Fig. 2A), a main photophase of 13.5 h is followed by a scotophase interrupted 1.5 h into the night by a 1-h light pulse (equivalent to point A), followed in different experimental subsets by a final dark period varying from 9.0 to 10.0 h in 15-min intervals (Lees, 1973). The results obtained show that the long-day effect (virginopara-production, or nondiapause development in the case of S. argyrostoma) elicited by the pulse falling on point A is over-ridden by a terminal dark period greater than the critical night length (9.5 h). In the second part of the experiment (Fig. 2B), an 8-h main photophase is followed by a 1-h scanning pulse placed, in different experimental subsets, 1–10 h after light off. In all cases, this pulse is then followed by a terminal dark period of 12 h, a value that exceeds the critical night length. The results show that long night effects (ovipara production M. viciae, or high incidence of diapause in S. argyrostoma) are apparent until the scanning pulse coincides with point B, 6–9 h after dusk, at which point short-night effects (virginopara production, or nondiapause production) are produced. Because each complex cycle includes a terminal dark period longer than the critical night length, it is apparent that the short-night effect of light falling on point B is irreversible.

image

Figure 2. The Lees experiment, originally designed to test night length measurement in the aphid Megoura viciae, although applied here to the induction of pupal diapause in the flesh fly Sarcophaga argyrostoma (Saunders, 1979). (A) Larvae of S. argyrostoma were exposed to complex four-component light:dark cycles comprising a 10-h ‘main’ photophase and a 1-h scanning pulse placed 3 h into the night at a position (point A) at which illumination causes nondiapause development. The scanning pulse is then followed by a terminal dark period varying from 7 to 13 h. Closed circles show phases of the photo-inducible phase (ϕi) calculated using the circadian rhythm of adult eclosion as a measure of phase (Saunders, 1979). When ϕi fell in the dark, diapause incidence was high; when it was phase delayed into the next photophase, diapause incidence was low. Diapause incidence (two experimental replicates) is shown in the small panel on the right. The results show that the diapause averting effect of light falling at point A is reversed by a terminal dark period longer than the critical night length (9.5 h). (B) Larvae exposed to cycles consisting of an 8-h ‘main’ photophase followed by 3–11 h of darkness, then a 1-h ‘scanning’ pulse and a final dark period (12 h) longer than the critical night length. When the scanning pulse coincided with ϕi(6–9 h after lights off) (a position equivalent to point B), diapause incidence was low. When ϕi fell in the dark, diapause supervened. The results show that illumination of point B cannot be reversed by a subsequent long night. These results are interpreted as evidence for ‘external coincidence’ in the photoperiodic clock, with point B marking the position of the photo-inducible phase (ϕi). ψx and ψy show alternative phase relationships between oscillator and the light cycle depending on the starting phase of the first light pulse in the train (Saunders, 1979).

Download figure to PowerPoint

Lees (1981) further examined differences between points A and B by exploring their spectral sensitivities. The action spectrum for point A shows a relatively narrow band of sensitivity mainly in the blue (450–470 nm). The action spectrum for point B, however, reveals a blue sensitivity extending into longer wavelengths almost as far as the red (600 nm). The results of these studies, when taken together with those for white light interruptions reported above, clearly show that interruptions early in the night are maximally sensitive to blue light and reversible by subsequent exposure to a long night, whereas interruptions late in the night show a spectral sensitivity extending into longer wavelengths, and a response that is not reversed by a subsequent long night. These results suggest that early night interruptions involve a single photoreceptor absorbing in the blue, whereas those in the latter half of the night probably involve at least two separate photoreceptors: one absorbing in the blue and the other at longer wavelengths.

Although the results for M. viciae suggest a noncircadian night-length timer, they share many characteristics with the photoperiodic responses of insects such as Sarcophaga spp., differing mainly in the absence of ‘positive’ resonance in Nanda-Hamner experiments (see below). It has been suggested, therefore, that the apparent hourglass-like response in M. viciae has its basis in the circadian system (Saunders & Lewis, 1987a), although the rhythmicity normally seen in Nanda-Hamner experiments is not expressed in the aphid, possibly because the circadian oscillator(s) that are involved in the response dampen below a threshold. Successive night lengths are not then registered as long nights in the greatly extended dark periods used in Nanda-Hamner experiments (Bünning, 1969; Lewis & Saunders, 1987; Saunders & Lewis, 1987a, b). Such a view is supported by observations that ‘positive’ resonance may be observed in other aphid species (Hardie, 1987) and (even in M. viciae) consecutive long nights appear to be accumulated in a repetitive or circadian fashion in some circumstances (Vaz Nunes & Hardie, 1993). This alternative circadian-based explanation is therefore presented below with reference to data for Sarcophaga spp.

Photoreception in flesh flies (Sarcophaga spp.)

  1. Top of page
  2. Abstract
  3. Introduction
  4. Models for the insect photoperiodic ‘clock’
  5. Photoreceptors at the organ level
  6. Spectral sensitivity of the photoperiodic response
  7. Photoreception in the parasitic wasp N. vitripennis
  8. Photoreception in the green vetch aphid M. viciae
  9. Photoreception in flesh flies (Sarcophaga spp.)
  10. What are the photopigments involved in insect photoperiodism?
  11. The evolution of photoperiodic clocks in insects and mites and their photoreceptive inputs
  12. Summary
  13. Acknowledgements
  14. References

Flesh flies (Sarcophaga spp.) are sensitive to the diapause-inducing effects of photoperiod during embryonic or larval development. For example, in S. crassipalpis, sensitivity is mainly in the intra-uterine embryos within gravid females (Denlinger, 1972), whereas, in S. argyrostoma, sensitivity is also embryonic but extends into the feeding larvae (Saunders, 1973). In S. similis, it extends as far as the post-feeding or ‘wandering’ larval stage (Goto & Numata, 2009). When these stages are exposed to the short nights of summer, successive generations of flies are produced that undergo uninterrupted development but, when exposed to the long nights of autumn, diapause supervenes in the pupa.

In S. argyrostoma, experimental evidence suggests strongly that the photoperiodic mechanism is rooted in the circadian system. This evidence has been reviewed previously (Saunders, 2010) and is not covered again in detail in the present review. Suffice to say, provided that the photophase is of sufficient duration and intensity, the circadian oscillation involved in the photoperiodic response is phase-set to a constant phase, equivalent to circadian time (CT) 12 h at the onset of darkness (Saunders, 2009), whereupon it commences its dark trajectory to measure the duration of the night. This oscillation then positions or ‘gates’ a photo-inducible phase (ϕi) to lie at the end of the critical night length. In S. argyrostoma, the critical night length is approximately 9.5 h, so that ϕi lies at approximately CT 21.5 h (Saunders, 1978). Under long nights, this phase falls in the dark, leading to diapause induction, whereas, under the short nights of summer, the dawn transition ‘tracks back’ to illuminate ϕi, leading to continuous nondiapause development. The model for S. argyrostoma, therefore, is of the external coincidence type (Fig. 3). In this model, pulses of light falling in the early subjective night (CT 12–18 h) cause phase delays (entrainment), eventually at point A, delaying the photo-inducible phase (ϕi) into the next photophase, thereby inducing nondiapause development. Pulses of light falling in the late subjective night (CT 18–24 h), on the other hand, cause phase advances (also entrainment) and then lead to photo-induction when the scanning pulse coincides directly with ϕi.

image

Figure 3. The external coincidence model for the photoperiodic clock (Pittendrigh, 1972). The circadian oscillation (shown here as a phase response curve) is reset to a constant phase (defined as Circadian time, CT 12 h) at the end of the photophase (vertical arrow). In (A) (long night cycle), the photo-inducible phase falls in the dark (closed circles), leading to the autumnal pathway (diapause induction); in (B) (short night cycle), the photo-inducible phase (open circles) is illuminated by the dawn transition of the daily photophase (open arrow) to give the summer developmental pathway (nondiapause development). Open horizontal arrows show the ‘movement’ of the dawn transition in relation to the oscillation as night length lengthens in the autumn (A) or shortens in early summer (B).

Download figure to PowerPoint

Tests for external coincidence in S. argyrostoma include the use of night interruptions that reveal the occurrence of the familiar bimodal response with two points of nondiapause: one (point A) early in the night and another (point B) late in the night (Saunders, 1975b). Application of the ‘Lees experiment' to such data (Saunders, 1981) produces results similar to those obtained in M. viciae (see above), in which point A is shown to be reversible by subsequent exposure to a long night, whereas nondiapause responses at point B prove to be irreversible by such treatment (Fig. 2). A similar result is also obtained for the whitefly A. proletella (Adams, 1986) and, more recently, for the flesh fly, S. similis (Goto & Numata, 2009).

A second test for external coincidence is the so-called ‘T-experiment' (Saunders, 1979), in which larvae of S. argyrostoma are exposed to a range of light/dark cycles ranging from LD 1 : 20.5 h (T 21.5) to LD 1 : 29.5 h (T 30.5), each containing a 1-h pulse of light and covering the primary range of entrainment for 1-h light pulses in this species (Saunders, 1979). The results show that only in a cycle of LD 1 : 20.5 h in which the light pulse illuminates the putative photo-inducible phase (at CT 21.5 h) (in computer simulations based upon the 1-h phase response curve) are low diapause or short-night effects observed. In all other cycles, CT 21.5 h falls in the dark, and diapause supervenes. The results of this and the earlier experiment leave little doubt that the photo-inducible phase lies late in the night at point B.

Studies on spectral sensitivity of flesh flies have been performed with all three Sarcophaga spp. considered in this review. Early observations with S. argyrostoma show that larvae are unable to distinguish 12 h of red light (>600 nm) from 18 h of red light per 24 h. The spectral sensitivity for the photoperiodic regulation of diapause in this species does not extend into these longer wavelengths (Saunders, 1973) as it does in N. vitripennis. A later test, with S. crassipalpis, shows that photosensitivity in the early part of the night is restricted to shorter wavelengths (green, approximately 540 nm) (Gnagey & Denlinger, 1984). Full action spectra for light breaks positioned both early and late in the scotophase, however, were then conducted with S. similis (Goto & Numata, 2009) in experiments exposing wandering larvae of S. similis to cycles of LD 12 : 12 h with a 2-h pulse of monochromatic light positioned either early in the night (at point A) or late in the night (at point B). An early light break shows maximum sensitivity to UV and blue light (395–470 nm) with no discernible effect in the yellow (583 nm) or the red (660 nm). By contrast, a light break positioned late in the night shows a much broader peak of sensitivity, ranging from 395 nm through blue (470 nm) to yellow (583 nm), with some response into the red end of the spectrum at 660 nm. These results prompted Goto & Numata (2009) to suggest that two separate photoreceptors are involved in S. similis, with a result similar to that recorded for M. viciae by Lees (1981), although markedly different from that in the parasitic wasp N. vitripennis (Saunders, 1975a, b).

Action spectra for the photoperiodic reaction have also been performed with at least three other species. In the nonbiting phantom midge Chaoborus americanus, monochromatic (green) light at 540 nm is most effective in terminating diapause when placed just after or just before the main photophase (Bradshaw, 1974). In the mosquito W. smithii, however, blue light (390–450 nm) is most effective at both dusk and dawn, although a ‘shoulder’ is also evident at longer wavelengths into the green (478–547 nm) (Bradshaw & Phillips, 1980). Early night interruptions (at point A) in the cabbage whitefly A. proletella show maximum sensitivity in the blue (410–420 nm), whereas those later in the night (at point B) also show evidence for a green photoreceptive pigment absorbing at 510–550 nm (Adams, 1986). Evidence for at least two photopigments is therefore suggested in W. smithii and A. proletella, resembling that in M. viciae and S. similis.

What are the photopigments involved in insect photoperiodism?

  1. Top of page
  2. Abstract
  3. Introduction
  4. Models for the insect photoperiodic ‘clock’
  5. Photoreceptors at the organ level
  6. Spectral sensitivity of the photoperiodic response
  7. Photoreception in the parasitic wasp N. vitripennis
  8. Photoreception in the green vetch aphid M. viciae
  9. Photoreception in flesh flies (Sarcophaga spp.)
  10. What are the photopigments involved in insect photoperiodism?
  11. The evolution of photoperiodic clocks in insects and mites and their photoreceptive inputs
  12. Summary
  13. Acknowledgements
  14. References

In principle, an action spectrum experimentally observed should correspond directly with the absorption spectrum of the involved pigment molecule, although the quality of the light reaching the photoreceptor may be modified by overlying tissues (Hardie et al., 1981) and, in parasitoids, by overlying host tissues (Claret, 1982). Nevertheless, in both M. viciae and S. similis, the spectral sensitivity of early light breaks (at point A) suggests the involvement of a photoreceptor absorbing short wavelength (blue) light. Because the external coincidence model suggests that light falling at this phase causes a phase delay of the photoperiodic oscillator, a strong candidate for this blue light receptor may be cryptochrome, a photoreceptor molecule that functions to reset (entrain) the circadian clock in D. melanogaster (Emery et al., 1998; Stanewsky et al., 1998) or perhaps a UV–blue absorbing opsin.

It is also suggested that opsins (i.e. opsin proteins conjugated with a vitamin A-based pigment) may act as photoperiodic photoreceptors in insects and mites. A range of different opsin species might thus be involved each responding to light of different spectral quality, with some of them absorbing at longer wavelength. Experimental evidence for such a role is provided by studies in which insects or mites are deprived of dietary carotenoids or vitamin A, with such treatment frequently eliminating or reducing the diapause-inducing effects of photoperiod, only for it to be reinstated by addition of the missing dietary components. Examples of such an effect are observed in mites (Veerman, 1980; Van Zon et al., 1981; Bosse & Veerman, 1996), Lepidoptera (Takeda, 1978; Shimizu & Kato, 1984; Claret, 1989) and Hymenoptera (Veerman et al., 1985). Of particular interest in the present context is the observation that vitamin A is found to be essential for the appearance of point B in the cabbage white butterfly Pieris brassicae (Claret & Volkoff, 1992), with point B in the external coincidence model being a phase sensitive to longer wavelength light.

Gao et al. (1999), working with M. viciae, used immunocytochemical techniques employing twenty antibodies raised against invertebrate and vertebrate opsins and proteins in the phototransduction cascade. Seven of these antibodies (including those raised against Drosophila rhodopsin 1, vertebrate opsins, vertebrate arrestin and general phototransduction components) consistently labelled a neuropile region of the brain previously identified as the likely site of photoreception by the use of light guides (Lees, 1964) and microcautery (Steel & Lees, 1977). The site of photoreception (and probably also the photoperiodic clock) in M. viciae is thus localized to a region of the protocerebrum lateral to the Group 1 neurosecretory cells, which are themselves considered to be the effectors controlling the photoperiodic regulation of seasonal morphs. In the silkmoth B. mori, Shimizu et al. (2001) also identified a novel brain-centred opsin (named boceropsin) that might be a longer wavelength photoreceptor involved in photoperiodism.

The data reviewed above suggest that multiple photoreceptors are involved in insect (and acarine) photoperiodic responses. In clocks of the external coincidence type, a short wavelength absorbing photoreceptor such as cryptochrome (or perhaps a UV–blue absorbing opsin) may be involved at both point A and at point B for entrainment of the photoperiodic oscillator, whereas longer wavelength absorbing opsins may constitute the diapause/nondiapause regulatory response at the photo-inducible phase (point B). In clocks of the internal coincidence type, however, opsins may be the dominant photoreceptors, either within brain tissues or in organized photoreceptors, such as the compound eyes (Goto et al., 2010).

This diversity in photoreception is to be expected given that there are multiple photoreceptors entraining behavioural circadian rhythms in D. melanogaster (Rieger et al., 2003) and, in insect photoperiodism itself, either retinal (compound eyes) or extraretinal (brain) photoreceptors appear to be involved (Numata & Hidaka, 1983; Bowen et al., 1984; Goto et al., 2010).

The evolution of photoperiodic clocks in insects and mites and their photoreceptive inputs

  1. Top of page
  2. Abstract
  3. Introduction
  4. Models for the insect photoperiodic ‘clock’
  5. Photoreceptors at the organ level
  6. Spectral sensitivity of the photoperiodic response
  7. Photoreception in the parasitic wasp N. vitripennis
  8. Photoreception in the green vetch aphid M. viciae
  9. Photoreception in flesh flies (Sarcophaga spp.)
  10. What are the photopigments involved in insect photoperiodism?
  11. The evolution of photoperiodic clocks in insects and mites and their photoreceptive inputs
  12. Summary
  13. Acknowledgements
  14. References

Photoperiodic diapause probably evolved on numerous occasions as insects (and mites) extended their distributions into higher latitudes with a pronounced winter season (Saunders, 2009). Because all insect photoperiodic mechanisms are probably circadian-based, their development from an earlier homodynamic life cycle in the tropics must have utilized the pre-existing (and ubiquitous) circadian system.

The best known circadian pacemaker is that in D. melanogaster, which regulates both adult locomotor activity and eclosion (Hall, 2003; Hardin, 2005; Sandrelli et al., 2008; Zhang & Emery, 2011). The transcriptional feedback loop underlying this rhythmicity involves a number of interacting ‘clock’ genes and their proteins. In short, after two key genes period (per) and timeless (tim) are transcribed, their proteins PERIOD (PER) and TIMELESS (TIM) build up in the cytoplasm during the night (or early subjective night in continuous darkness) where they form a heterodimer (PER/TIM) that subsequently re-enters the nucleus to act as a negative regulator of the CYCLE/CLOCK (CYC/CLK) dimer, which is itself responsible for per and tim transcription. Entrainment of this Drosophila pacemaker is effected by blue light absorbing CRYPTOCHROME, a dedicated circadian photoreceptor, encoded by cryptochrome1 (cry1), and binding directly to TIM, causing its degradation (Emery et al., 1998; Stanewsky et al., 1998; Ceriani et al., 1999; Busza et al., 2004). Such degradation leads to an associated degradation of PER. If this happens early in the night, when PER and TIM are on the upswing, the oscillation undergoes a phase delay; if it occurs later in the night, when PER and TIM are declining, it causes a phase advance.

The molecular events described above may also occur in other higher Diptera (e.g. Sarcophaga spp.; M. Meuti, personal communication), although they are not representative of the phenomenon in all insects. In the monarch or milkweed butterfly Danaus plexippus, ‘mammalian-type’ CRY2 is present, as well as the dedicated photoreceptor or ‘Drosophila-type’ CRY1 (Merlin & Reppert, 2010). CRY2 acts as a transcriptional repressor of the CYC/CLK dimer as part of the autoregulatory feedback loop itself.

Zhan et al. (2011) recently surveyed the occurrence of five important ‘clock’ genes [per, cry1, cry2, tim1 and tim2 (timeout)] in 18 species of insects whose genomes have been elucidated. All five genes were found in two species of Lepidoptera (Bombyx mori and D. plexippus), in three mosquitoes (Anopheles gambiae, Aedes aegypti and Culex quinquefasciatus), and in the aphid Acyrthosiphon pisum. In two species of Drosophila (D. melanogaster and Drosophila pseudoobscura), cry2 is absent, whereas, in five species of Hymenoptera, including N. vitripennis, cry1 and tim1 are both absent. CRY2 is also found in the bean bug Riptortus pedestris (Ikeno et al., 2011).

The form of the clock containing cry2 (encoding CRY2) is regarded as ‘ancestral’ (Yuan et al., 2007; Sandrelli et al., 2008; Merlin & Reppert, 2010; Tomioka & Matsumoto, 2010), whereas that in D. melanogaster, in which CRY2 has been lost, and that in the honey bee Apis mellifera (Rubin et al., 2006) and in N. vitripennis (Schurko et al., 2010), in which both CRY1 and TIM have been lost, are considered to be ‘derived’.

If these differences also occur in the photoperiodic mechanism, substantial differences in the way that clock genes are involved in photoperiodism may also be expected (Saunders & Bertossa, 2011). For example, in higher flies (e.g. Sarcophaga spp.; considered here to represent an example of external coincidence) blue-light absorbing cryptochrome (CRY1) may be involved in phase-setting (entraining) the photoperiodic oscillator, whereas opsin-based photoreceptors absorbing longer wavelength light may be responsible for operating the diapause/nondiapause switch when light coincides with the photo-inducible phase. However, in N. vitripennis (considered here to represent an example of internal coincidence), where CRY1 is absent and CRY2 has a nonphotoreceptive function, entrainment of both dawn and dusk oscillators may be through the agency of opsins absorbing at a variety of wavelengths. In different species, these opsins may be in the brain or the compound eyes. It is concluded that much more research is needed on photoreceptors at both the organ and molecular levels to determine their role in photoperiodism.

Summary

  1. Top of page
  2. Abstract
  3. Introduction
  4. Models for the insect photoperiodic ‘clock’
  5. Photoreceptors at the organ level
  6. Spectral sensitivity of the photoperiodic response
  7. Photoreception in the parasitic wasp N. vitripennis
  8. Photoreception in the green vetch aphid M. viciae
  9. Photoreception in flesh flies (Sarcophaga spp.)
  10. What are the photopigments involved in insect photoperiodism?
  11. The evolution of photoperiodic clocks in insects and mites and their photoreceptive inputs
  12. Summary
  13. Acknowledgements
  14. References

Studies on spectral sensitivity provide circumstantial evidence that two classes of photoreceptor (i.e. cryptochrome and opsins) qualify as photoreceptors in insect photoperiodism. The clock gene cryptochrome thus emerges as one of the potentially important elements in the photoperiodic mechanism. For example, in external coincidence types of clock (exemplified by species of Sarcophaga and possibly other higher Diptera), a blue-sensitive photoreceptor such as CRY1 may be responsible for the entrainment of the photoperiodic oscillator, whereas photoreceptors sensitive to longer wavelengths, possibly opsins, are involved in the diapause/nondiapause switch in metabolism, which occurs when light coincides with the photo-inducible phase. A similar type of clock may operate in the aphid M. viciae. In internal coincidence types of clock, on the other hand, as in N. vitripennis, entrainment may be regulated by photoreceptors absorbing at longer wavelengths, which, in the absence of a photoreceptive or ‘Drosophila type’ CRY1, may also be opsin-based. In the ‘ancestral’ photoperiodic clock of the Lepidoptera where both CRY1 and CRY2 are present, the photoperiodic clock may present properties of both internal and external coincidence. Further investigations of the importance of cryptochromes in insect photoperiodism will require additional comparative studies of clock genes in sequenced insect genomes and gene ‘silencing’ (RNAi) studies, especially in those species with pronounced photoperiodic responses.

Acknowledgements

  1. Top of page
  2. Abstract
  3. Introduction
  4. Models for the insect photoperiodic ‘clock’
  5. Photoreceptors at the organ level
  6. Spectral sensitivity of the photoperiodic response
  7. Photoreception in the parasitic wasp N. vitripennis
  8. Photoreception in the green vetch aphid M. viciae
  9. Photoreception in flesh flies (Sarcophaga spp.)
  10. What are the photopigments involved in insect photoperiodism?
  11. The evolution of photoperiodic clocks in insects and mites and their photoreceptive inputs
  12. Summary
  13. Acknowledgements
  14. References

Drs Steven Reppert, David Denlinger and Shin Goto are thanked for their helpful comments on the manuscript, and Megan Meuti is thanked for providing preliminary information on cryptochromes in Sarcophaga spp. and other ‘higher’ Diptera. Professor R. M. K. Saunders is also thanked for help with the production of the figures.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Models for the insect photoperiodic ‘clock’
  5. Photoreceptors at the organ level
  6. Spectral sensitivity of the photoperiodic response
  7. Photoreception in the parasitic wasp N. vitripennis
  8. Photoreception in the green vetch aphid M. viciae
  9. Photoreception in flesh flies (Sarcophaga spp.)
  10. What are the photopigments involved in insect photoperiodism?
  11. The evolution of photoperiodic clocks in insects and mites and their photoreceptive inputs
  12. Summary
  13. Acknowledgements
  14. References
  • Adams, A.J. (1986) Night-interruption experiments and action spectra for dawn and dusk in relation to the photoperiodic clock of the cabbage whitefly, Aleyrodes proletella (Hemiptera: Aleyrodidae). Journal of Insect Physiology, 32, 7178.
  • Berlinger, M.J. & Ankersmit, G.W. (1976) Manipulation with the photoperiod as a method of control of Adoxophyes orana (Lepidoptera: Tortricidae). Entomologia Experimentalis et Applicata, 19, 96107.
  • Bosse, T.C. & Veerman, A. (1996) Involvement of vitamin A in the photoperiodic induction of diapause in the spider mite Tetranychus urticae is demonstrated by rearing an albino mutant on a semi-synthetic diet with and without β-carotene or vitamin A. Physiological Entomology, 21, 181192.
  • Bowen, M.F., Saunders, D.S., Bollenbacher, W.E. & Gilbert, L.I. (1984) In vitro reprogramming of the photoperiodic clock in an insect brain-retrocerebral complex. Proceedings of the National Academy of Sciences of the United States of America, 81, 58815884.
  • Bradshaw, W.E. (1972) Action spectra for photoperiodic response in a diapausing mosquito. Science, 175, 13611362.
  • Bradshaw, W.E. (1974) Photoperiodic control of development in Chaoborus americanus with special reference to photoperiodic action spectra. Biological Bulletin, 146, 1119.
  • Bradshaw, W.E. & Phillips, D.L. (1980) Photoperiodism and the photic environment of the pitcher-plant mosquito, Wyeomyia smithii. Oecologia (Berlin), 44, 311316.
  • Bünning, E. (1936) Die endogene tagesrhythmik als grundlage der photoperiodischen reaktion. Berichte der Deutschen Botanischen Gesellschaft, 54, 590607.
  • Bünning, E. (1969) Common features of photoperiodism in plants and animals. Photochemistry and Photobiology, 9, 219228.
  • Bünning, E. & Joerrens, G. (1960) Tagesperiodische antagonistische Schwankungen der Blau-violett und Gelbrot-Empfindlichkeit als Grundlage der photoperiodischen Diapause-Induktion bei Pieris brassicae. Zeitschrift fur Naturforschung, 15, 205213.
  • Busza, A., Emery-Le, M., Rosbash, M. & Emery, P. (2004) Roles of two Drosophila CRYPTOCHROME structural domains in circadian photoreceptors. Science, 304, 15031506.
  • Ceriani, M.F., Darlington, T.K., Staknis, D. et al. (1999) Light-dependent sequestration of TIMELESS by CRYPTOCHROME. Science, 285, 553556.
  • Claret, J. (1966) Recherche du centre photorecepteur lors de l’induction de la diapause chez Pieris brassicae L. Comptes Rendus de l’Académie des Sciences, 262, 14641465.
  • Claret, J. (1972) Sensibilité spectrale des chenilles de Pieris brassicae (L.) lors de l’induction photoperiodique de la diapause. Comptes Rendus de l’Académie des Sciences (Paris), Série D, 274, 17271730.
  • Claret, J. (1982) Modification du signal photopériodique par la cuticle de l'hôte pour un endoparasite. Comptes Rendus des Séances Société de Biologie et de ses Filiales (Paris), 176, 834838.
  • Claret, J. (1989) Vitamin A et induction photoperiodique ou thermopériodique de la diapause chez Pieris brassicae. Comptes Rendus de l’ Académie Sciences Série III, 308, 347352.
  • Claret, J. & Volkoff, N. (1992) Vitamin A is essential for two processes involved in the photoperiodic reaction in Pieris brassicae. Journal of Insect Physiology, 38, 569574.
  • Cymborowski, B., Lewis, R.D., Hong, S.-F. & Saunders, D.S. (1994) Circadian locomotor activity rhythms and their entrainment by light-dark cycles continues in flies (Calliphora vicina) surgically deprived of their optic lobes. Journal of Insect Physiology, 40, 501510.
  • Denlinger, D.L. (1972) Embryonic determination of pupal diapause in the flesh fly Sarcophaga crassipalpis. Journal of Insect Physiology, 17, 18151822.
  • De Wilde, J. & Bonga, H. (1958) Observations on threshold intensity and sensitivity of different wavelengths of photoperiodic response in the Colorado beetle (Leptinotarsa decemlineata Say). Entomologia Experimentalis et Applicata, 1, 301307.
  • Dickson, R.C. (1949) Factors governing the induction of diapause in the oriental fruit moth. Annals of the Entomological Society of America, 42, 511537.
  • Emery, P., So, W.V., Kaneko, M. et al. (1998) CRY, a Drosophila clock and light-regulated cryptochrome, is a major contributor to circadian rhythm resetting and photosensitivity. Cell, 95, 669679.
  • Ferenz, H.J. (1975) Photoperiodic and hormonal control of reproduction in male beetles, Pterostichus nigrita. Journal of Insect Physiology, 21, 331341.
  • Gao, N., von Schantz, M., Foster, R.G. & Hardie, J. (1999) The putative brain photoreceptors in the vetch aphid, Megoura viciae. Journal of Insect Physiology, 45, 10111019.
  • Geispitz, K.F. (1957) The mechanism of acceptance of light stimuli in the photoperiodic reaction of Lepidoptera larvae. Zoologicheskii zhurnal, 36, 548560 (In Russian).
  • Gelman, D.B. & Hayes, D.K. (1980) Physical and biochemical factors affecting diapause in insects, especially in the European corn borer, Ostrinia nubilalis. Physiological Entomology, 5, 367383.
  • Gnagey, A.L. & Denlinger, D.L. (1984) Photoperiodic induction of pupal diapause in the flesh fly, Sarcophaga crassipalpis: embryonic sensitivity. Journal of Comparative Physiology B, 154, 9196.
  • Goto, S.G. & Numata, H. (2009) Possible involvement of distinct photoreceptors in the photoperiodic induction of diapause in the flesh fly Sarcophaga similes. Journal of Insect Physiology, 55, 401407.
  • Goto, S.G., Shiga, S. & Numata, H. (2010) Photoperiodism in insects: perception of light and the role of clock genes. Photoperiodism: The Biological Calendar (ed. by R. J. Nelson, D. L. Denlinger and D. E. Somers), pp. 258286. Oxford University Press, New York, New York.
  • Hall, J.C. (2003) Genetics and molecular biology of rhythms in Drosophila and other insects. Advances in Genetics, 48, 1280.
  • Hardie, J. (1987) The photoperiodic control of wing development in the black bean aphid, Aphis fabae. Journal of Insect Physiology, 33, 543549.
  • Hardie, J. (2010) Photoperiodism in insects: aphid polyphenism. Photoperiodism: The Biological Calendar (ed. by R. J. Nelson, D. L. Denlinger and D. E. Somers), pp. 342363. Oxford University Press, New York, New York.
  • Hardie, J., Lees, A.D. & Young, S. (1981) Light transmission through the head capsule of an aphid, Megoura viciae. Journal of Insect Physiology, 27, 773777.
  • Hardin, P.E. (2005) The circadian timekeeping system of Drosophila. Current Biology, 15, R714R722.
  • Harris, F.A., Lloyd, E.P., Lane, H.C. & Burt, E.C. (1969) Influence of light on diapause in the boll weevil. II. Dependence of diapause response on various bands of visible radiation and a broad band of infrared radiation used to extend the photoperiod. Journal of Economic Entomology, 62, 854857.
  • Hasegawa, K. & Shimizu, I. (1987) In vivo and in vitro photoperiodic induction of diapause using isolated brain-suboesophageal ganglion complexes of the silkworm, Bombyx mori. Journal of Insect Physiology, 33, 959966.
  • Ikeno, T., Numata, H. & Goto, S.G. (2011) Photoperiodic response requires mammalian-type cryptochrome in the bean bug Riptortus pedestris. Biochemical and Biophysical Research Communications, 410, 394397.
  • Kogure, M. (1933) The influence of light and temperature on certain characters of the silk worm, Bombyx mori. Journal of the Department of Agriculture, Kyushu University, 4, 193.
  • Koštál, V. (2011) Insect photoperiodic calendar and circadian clock: independence, cooperation, or unity? Journal of Insect Physiology, 57, 538556.
  • Kriegsfeld, L.J. & Bittman, E.L. (2010) Photoperiodism and reproduction in mammals. Photoperiodism: The Biological Calendar (ed. by R.J. Nelson, D.L. Denlinger and D.E. Somers), pp. 503542. Oxford University Press, New York, New York.
  • Lees, A.D. (1953) Environmental factors controlling the evocation and termination of diapause in the fruit tree spider mite Metatetranychus ulmi Koch (Acarina: Tetranychidae). Annals of Applied Biology, 40, 449486.
  • Lees, A.D. (1964) The location of the photoperiodic receptors in the aphid Megoura viciae. Journal of Experimental Biology, 41, 119133.
  • Lees, A.D. (1971) The relevance of action spectra in the study of insect photoperiodism. Biochronometry (ed. by M. Menaker), pp. 372380. National Academy of Sciences, Washington, District of Columbia.
  • Lees, A.D. (1973) Photoperiodic time measurement in the aphid Megoura viciae. Journal of Insect Physiology, 19, 22792316.
  • Lees, A.D. (1981) Action spectra for the photoperiodic control of polymorphism in the aphid Megoura viciae. Journal of Insect Physiology, 27, 761771.
  • Lees, A.D. (1986) Some effects of temperature on the hour glass photoperiod timer in the aphid Megoura viciae. Journal of Insect Physiology, 32, 7989.
  • Lewis, R.D. & Saunders, D.S. (1987) A damped circadian oscillator model of an insect photoperiodic clock. I. Description of the model based on a feedback control system. Journal of Theoretical Biology, 128, 4759.
  • Merlin, C. & Reppert, S.M. (2010) Lepidopteran circadian clocks. From molecules to behavior. Molecular Biology and Genetics of the Lepidoptera (ed. by M. R. Goldsmith and F. Marec), pp. 137152. CRC Press, Boca Raton, Florida.
  • Morita, A. & Numata, H. (1999) Localization of the photoreceptor for photoperiodism in the stink bug, Plautia stali. Physiological Entomology, 24, 190196.
  • Müller, H.J. (1964) Uber die Wirkung Verschiedener Spektralbereichebei der photoperiodischen Induktion der Saisonformen von Euscelis plebejus Fall. (Homoptera: Jassidae). Zoologisches Jahrbucher Abteilung für Allgemeine Zoologie und Physiologie der Tiere, 70, 411426.
  • Nanda, K.K. & Hamner, K.C. (1958) Studies on the nature of the endogenous rhythm affecting photoperiodic response of Biloxi soybean. Botanical Gazette, 120, 1425.
  • Nishizuka, M., Azuma, A. & Masaki, S. (1998) Diapause response to photoperiod and temperature in Lepisma saccharina Linnaeus (Thysanura: Lepismatidae). Entomological Science, 1, 714.
  • Norris, K.H., Howell, F., Hayes, D.K. et al. (1969) The action spectrum for breaking diapause in the codling moth, Laspeyresia pomonella (L.), and the oak silkworm, Antheraea pernyi Guer. Proceedings of the National Academy of Sciences of the United States of America, 63, 11201127.
  • Numata, H. & Hidaka, T. (1983) Compound eyes as the photoperiodic receptors in the bean bug. Experientia, 39, 868869.
  • Pittendrigh, C.S. (1966) The circadian oscillation in Drosophila pseudoobscura pupae: a model for the photoperiodic clock. Zeitschrift für Pflanzenphysiologie, 54, 275307.
  • Pittendrigh, C.S. (1972) Circadian surfaces and the diversity of possible roles of circadian organization in photoperiodic induction. Proceedings of the National Academy of Sciences of the United States of America, 69, 27342737.
  • Pittendrigh, C.S. & Minis, D.H. (1964) The entrainment of circadian oscillations by light and their role as photoperiodic clocks. American Naturalist, 98, 261294.
  • Pittendrigh, C.S., Eichhorn, J.H., Minis, D.H. & Bruce, V.G. (1970) Circadian systems VI. Photoperiodic time measurement in Pectinophora gossypiella. Proceedings of the National Academy of Sciences of the United States of America, 66, 758764.
  • Rieger, D., Stanewsky, R. & Helfrich-Forster, C. (2003) 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. Journal of Biological Rhythms, 18, 377391.
  • Roenneberg, T., Radic, T., Gödel, M. & Merrow, M. (2010) Seasonality and photoperiodism in fungi. Photoperiodism: The Biological Calendar (ed. by R. J. Nelson, D. L. Denlinger and D. E. Somers), pp. 134163. Oxford University Press, New York, New York.
  • Rubin, E.B., Shemesh, Y., Cohen, M. et al. (2006) Molecular and phylogenetic analyses reveal mammalian-like clockwork in the honey bee (Apis mellifera) and shed new light on the molecular evolution of the circadian clock. Genome Research, 16, 13521365.
  • Sandrelli, F., Costa, R., Kyriacou, C.P. & Rosato, E. (2008) Comparative analysis of circadian clock genes in insects. Insect Molecular Biology, 17, 447463.
  • Saunders, D.S. (1966) Larval diapause of maternal origin-II. The effect of photoperiod and temperature on Nasonia vitripennis. Journal of Insect Physiology, 12, 569581.
  • Saunders, D.S. (1973) The photoperiodic clock in the flesh fly, Sarcophaga argyrostoma. Journal of Insect Physiology, 19, 19411954.
  • Saunders, D.S. (1974) Evidence for ‘dawn’ and ‘dusk’ oscillators in the Nasonia photoperiodic clock. Journal of Insect Physiology, 20, 7788.
  • Saunders, D.S. (1975a) Spectral sensitivity and intensity thresholds in Nasonia photoperiodic clock. Nature, 253, 732734.
  • Saunders, D.S. (1975b) ‘Skeleton’ photoperiods and the control of diapause and development in the flesh-fly, Sarcophaga argyrostoma. Journal of Comparative Physiology, 97, 97112.
  • Saunders, D.S. (1978) Internal and external coincidence and the apparent diversity of photoperiodic clocks in the insects. Journal of Comparative Physiology, 127, 197207.
  • Saunders, D.S. (1979) External coincidence and the photoinducible phase in the Sarcophaga photoperiodic clock. Journal of Comparative Physiology, 132, 179189.
  • Saunders, D.S. (1981) Insect photoperiodism: entrainment within the circadian system as a basis for time measurement. Biological Clocks in Seasonal Reproductive Cycles (ed. by B. K. Follett), pp. 6781. John Wright & Sons, U.K.
  • Saunders, D.S. (2002) Insect Clocks, 3rd edn. Elsevier, The Netherlands.
  • Saunders, D.S. (2009) Circadian rhythms and the evolution of photoperiodic timing in insects. Physiological Entomology, 34, 301308.
  • Saunders, D.S. (2010) Photoperiodism in insects: migration and diapause responses. Photoperiodism: The Biological Calendar (ed. by R. J. Nelson, D. L. Denlinger and D. E. Somers), pp. 218257. Oxford University Press, New York, New York.
  • Saunders, D.S. (2011) Unity and diversity in the insect photoperiodic mechanism. Entomological Science, 14, 235244.
  • Saunders, D.S. & Bertossa, R.C. (2011) Deciphering time measurement: the role of circadian ‘clock’ genes and formal experimentation in insect photoperiodism. Journal of Insect Physiology, 57, 557566.
  • Saunders, D.S. & Cymborowski, B. (1996) Removal of optic lobes of adult blow flies (Calliphora vicina) leaves photoperiodic induction of larval diapause intact. Journal of Insect Physiology, 42, 807811.
  • Saunders, D.S. & Lewis, R.D. (1987a) A damped circadian oscillator model of an insect photoperiodic clock. II. Simulations of the shapes of the photoperiodic response curve. Journal of Theoretical Biology, 128, 6171.
  • Saunders, D.S. & Lewis, R.D. (1987b) A damped oscillator model of an insect photoperiodic clock. III. Circadian and ‘hourglass’ responses. Journal of Theoretical Biology, 128, 7385.
  • Schurko, A.M., Mazur, D.J. & Logsdon, J.M. (2010) Inventory and phylogenomic distribution of meiotic genes in Nasonia vitripennis and among diverse arthropods. Insect Molecular Biology, 19, 165180.
  • Shiga, S. & Numata, H. (1997) The adult blow fly (Protophormia terraenovae) perceives photoperiod through the compound eyes for the induction of reproductive diapause. Journal of Comparative Physiology A, 181, 3540.
  • Shimizu, I. & Kato, M. (1984) Carotenoid functions in photoperiodic induction in the silkworm, Bombyx mori. Photobiochemistry and Photobiophysics, 7, 4752.
  • Shimizu, I., Yamakawa, Y., Shimazaki, Y. & Iwasa, T. (2001) Molecular cloning of Bombyx cerebral opsin (Boceropsin) and cellular localization of its expression in the silkworm brain. Biochemical and Biophysical Research Communications, 287, 2734.
  • Shintani, Y. & Numata, H. (2009) Different photoreceptor organs are used for photoperiodism in the larval and adult stages of the carabid beetle, Leptocarabus kumagaii. Journal of Experimental Biology, 212, 36513655.
  • Stanewsky, R., Kaneko, M., Emery, P. et al. (1998) The cryb mutation identifies cryptochrome as a circadian photoreceptor in Drosophila. Cell, 95, 681692.
  • Steel, C.G.H. & Lees, A.D. (1977) The role of neurosecretion in the photoperiodic control of polymorphism in the aphid Megoura viciae. Journal of Experimental Biology, 67, 117135.
  • Suzuki, T., Fukanaga, Y., Amano, H. et al. (2008) Effects of light quality and intensity on diapause induction in the two-spotted spider mite, Tetranychus urticae. Applied Entomology and Zoology, 43, 213218.
  • Takeda, M. (1978) Photoperiodic time measurement and seasonal adaptation of the south-western corn borer, Diatraea grandiosella Dyar (Lepidoptera: Pyralidae). PhD Thesis, University of Missouri.
  • Tomioka, K. & Matsumoto, A. (2010) A comparative view of insect clock systems. Cellular and Molecular Life Sciences, 67, 13971406.
  • Van Zon, A.Q., Overmeer, W.P.J. & Veerman, A. (1981) Carotenoids are functionally involved in photoperiodic induction of diapause in a predacious mite. Science, 213, 11311133.
  • Vaz Nunes, M. & Hardie, J. (1993) Circadian rhythmicity is involved in photoperiodic time measurement in the aphid Megoura viciae. Experientia, 49, 711713.
  • Vaz Nunes, M. & Saunders, D.S. (1999) Photoperiodic time measurement in insects: a review of clock models. Journal of Biological Rhythms, 14, 84104.
  • Veerman, A. (1980) Functional involvement of carotenoids in photoperiodic induction of diapause in the spider mite. Physiological Entomology, 5, 291300.
  • Veerman, A., Slagt, M.E., Alderliest, M.F.J. & Veenendaal, R.L. (1985) Photoperiodic induction of diapause in an insect is vitamin A dependent. Experientia, 41, 11941195.
  • Williams, C.M. (1963) Control of pupal diapause by the direct action of light on the insect brain. Science, 140, 386.
  • Williams, C.M. & Adkisson, P.L. (1964) Physiology of insect diapause XIV. An endocrine mechanism for the photoperiodic control of pupal diapause in the oak silkworm, Antheraea pernyi. Biological Bulletin of the Marine Laboratories, Woods Hole, 127, 511525.
  • Williams, C.M., Adkisson, P.L. & Walcott, C. (1965) Physiology of insect diapause XV. The transmission of photoperiodic signals to the brain of the oak silkworm, Antheraea pernyi. Biological Bulletin of the Marine Biological Laboratories, Woods Hole, 128, 497507.
  • 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. Molecular Biology and Evolution, 24, 948955.
  • Zhan, S., Merlin, C., Boone, J.L. & Reppert, S.M. (2011) The monarch butterfly genome yields insights into long-distance migration. Cell, 147, 11711185.
  • Zhang, Y. & Emery, P. (2011) Molecular and neural control of insect circadian rhythms. Insect Molecular Biology and Biochemistry (ed. by L. I. Gilbert), pp. 513551. Elsevier, The Netherlands.