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Insect Circadian Rhythms and Photoperiodism

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Insect Circadian Rhythms and Photoperiodism Invertebrate Neuroscience, 3,155-164 (1997) Insect circadian rhythms and photoperiodism D. S. SAUNDERS Institute of Cell, Animal and Population Biology, University of Edinburgh, West Mains Road, Edinburgh EH9 3JT ABSTRACT Two clock-controlled processes, overt circadian rhythmicity and the photoperiodic induction of dia- pause, 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 'cas- cade' 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 intercere- bralis region of the mid-brain. KEY WORDS: Circadian; photoperiod; diapause; photoreception; time measurement Introduction of the clocks within the central nervous system, and their regulation at the cellular level. Insects display a large number of behavioural, develop- mental and physiological events which are controlled by endogenous clock-like processes. Among the Circadian rhythms of locomotor activity 'higher' Diptera, for example, an array of daily behav- iours such as general locomotor activity, flight, mating, Rhythms of locomotor activity in Calliphora vicina are oviposition, egg hatch, pupariation and pupal eclosion easily recorded by placing a fly in a 9 cm petri dish are governed by circadian oscillators, whereas various with a supply of sugar and water, in such a way that seasonal phenomena such as the onset of diapause, or the moving fly breaks an infra-red light beam. These larval growth rates, are governed by photoperiodic events are registered by computer and presented as clocks (Saunders, 1982). This review is concerned conventional 'double-plotted' actograms (Fig. 1). with circadian rhythms and photoperiodism in the The actograms shown in Fig. 1 illustrate four cardi- adults of two species, the blow fly Calliphora vicina, and nal properties of a circadian rhythm (for a day-active the fruit fly Drosophila melanogaster. Both species show insect): (1) In continuous darkness (DD) and constant rhythms of locomotor activity whose properties are temperature (20~ an adult fly presents a noise-free well-known (e.g. Kenny and Saunders, 1991; Saunders and free-running rhythm of activity and rest which may et al., 1994) and whose regulatory mechanisms are persist for up to 7 weeks (Fig. 1A). Although close to beginning to be unravelled (e.g. Hall, 1995). In addi- 24 h, the period (*) of the rhythm varies in individual tion, the blow fly overwinters in a larval diapause flies from about 21 to 25 h, with a mean value of about (Saunders, 1987), whereas D. melanogaster is known to 22.5 h (Cymborowski et al., 1993). (2) Step-wise possess a very shallow ovarian diapause (Saunders changes in temperature, either down or up, cause phase et al., 1989, 1990) which may aid overwintering sur- shifts of the rhythm, but otherwise leave ~ unaltered, vival in some populations (Saunders and Gilbert, attesting to its temperature-compensation (Fig. 1B). 1990). The two clock-like phenomena will be com- (3) When a fly is exposed to a cycle of light and dark- pared, and questions asked about their similarities and ness (in this case LD 16:8) the activity rhythm differences, the photoreceptors involved, the location becomes entrained to an exact 24 h with locomotion Corresponding author: D. S. Saunders. E-mail: [email protected] 15 6 Saunders largely restricted to the light (Fig. 1C). Lastly (4), Fewer than 5 per cent of flies show spontaneous transfer from DD to continuous 'bright' light (LL) leads 'splitting' of activity in DD (Kenny and Saunders, to behavioural arrhythmicity (Fig. 1D), although LL 1991) or when exposed to a light cycle of LD 1:23 below about 0.02 Wm "z causes z to lengthen (Hong with the light pulse coming on in the middle of the and Saunders, 1994). 'subjective night' (Hong and Saunders, in press) B Time h 14.00 02.00 14.00 02.00 14.00 23 h ..... i, !k..:,• :" a ..... A lqme h Day 1 ii lit , ,, 12.00 24.00 12.00 24.00 12.00 il6M i '~ ~'"v i"ii '....... Iil I i~Ll!'l;lli!!i':~[ Day 1 ILt~IamiMi ~I 'W ~&k'i~'g'~" LI,d ~.,~ ..... IN ill a i~ fill ili~i ~o ~s m ~s a~ 7 il lii i F I~" Period {h} \: ,ilii 23.3 h [ 1 4 ll/lu i~. i Im~ /!13.3 h 7 = ~ I~* ..ilila, i a r ~--~- b ii i illiL J a n ,i ~- .I,; ..... lllll ,e,iu~ c 14: i i i ua e II lit i ,liiJ Jill, blij /~ ~o ~s 2o as ao Penod {h} Period #'4 14|I t, ",i'u'~ I, i ~..~,~ '~ ,i.~lltU~jinl ~ ,.,.,u,kak~.,. , i~ it,. i~ild li-"~" .i :--""', 23.3 h 21 ~ .~ ..... t.*aka&L_ 21 , ,,,h ,;....,~...~. ~. 28: Period (h) C Time h ~me h 12.~ 24.~ 12.~ 24.~ 12.~ 22.7 h D ~5.oo 3.oo ~5.oo 3.00 15.00 Day 22.7 h Day a! r ~,,. wu, I" i~, a tiiJl ~Jilll 'i ~ J/lllli[ J|llJli Jnl a a AiJ~, hJ dmlJl I n dillil I ,,~/i I r e 7 JdUI it i=i ~ltlgL ,~lK~lki, iiM~ / Pe[iod (h) Jh/i t J ~ ~lIL t.,, ......... ,,,,,, ...... a 7 |kkMlmlJ hbJJ~d, ,l~.u .... J, a 10 15 2o 25 3c r [i~ail~, .L,~U... ..... .~, .a, Jv Penc<l lhl L a n e Period (h) o h ' --. a,. _ ,id,,~ .~ , i,.,,,~ =, ' d J c 10 15 20 25 30 L .... dL~J .,~I t , ,,,a.,~t,. ,.-~ ,~, la|i P~nod (hl 23.3 h #hdkd v Period (h} r Jl ~' i i~ c a i I~ ill , n .... iMt , ~l ..... c o ,iJa .~all~ 10 15 20 ~ 30 28 ~#i Penc<l(h) Fig. 1. CaUiphora vicina. Actograms showing circadian locomotor activity rhythms of single females. A - 'free running' rhythm in continuous darkness (DD), 20~ B - ditto, with step-wise temperature changes from 20~ to 15~ on day 8 (arrow) and from 15 ~ to 25~ on day 18 (arrow). C - fly initially in DD, exposed to an entraining cycle of LD 16:8 from days 8 to 14, and then back to DD. Arrow shows 'rebound' of activity shortly after light.off. D -fly initially in DD, then exposed to continuous bright light (0.024 Wm "2) from day 8 to 18, and then back to DD. Periodogram analyses for appropriate sections of the records are shown alongside each paneL Insect circadian rhythms and photoperiodism 15 7 (Fig. 2). Interpretation of these observations is that expressed rhythms with a period (,) close to 19 h, a long circadian rhythmicity is a multi-oscillator (and proba- period mutant (perL) a period close to 29 h, and a third bly multicellular) phenomenon. class of mutants (per~ which were apparently arrhyth- mic. This important and seminal study described the first 'clock' mutants in any organism and set the scene for the considerable subsequent successes in unravelling Time h the molecular genetics of the circadian system in Drosophila (see Hall, 1995, 1996). In our hands 12.00 24.00 12.00 24.00 12.00 (Saunders et al., 1994) the mean circadian period of pers Day ifllJfll !~trl[!rl[_ 1LI jr! i /,It/ _ ~_i/~L was found to be 19.70 + 0.57 h, per+ 23.72 + 0.90 h and perL2 29.10 + 3.64 h (in all cases, N = 50, mean + SD). i~ ili~lb i ,iiiili~ii pers was characterised by a shortened active phase, and i JiiliLL~ ~Jillll|,il a perL2 by a lengthened rest phase. Representative exam- lllli, ii ,~llil~ll ples of these mutant rhythms are shown in Fig. 3. ,~sllliill iJ il i Mutation at a second 'clock' locus, timeless (tim) il il i li ,lllil, has been found to abolish circadian rhythmicity in 7i i.i ili,~, itl li!i i -- i D. melanogaster (Vosshall et al., 1994). The proposed ' hi ii~ , tii~ ill interactions between the PER and TIM proteins in the it, i li~i Q.! [~.I@| | generation of circadian rhythmicity is discussed later. ,, [,i Photoperiodic induction of larval diapause ,i t/C,t,u', i ~ ,,t ,Jill,i,/! b in Calliphora vicina 141 i . i illil,i~ ~ i ,, mill Lt I Adult females of C. vicina, entrained to daily light- dark cycles, use a photoperiodic 'clock' measuring ,,i Jll ,,_ ..... i,r,i daylength (or night length) to regulate the onset of an ,, , ..... , overwintering larval diapause. Thus flies exposed to I the long days (or short nights) of summer produce a I u F~ succession of continuously developing generations 21[l ~.
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