A Comparative Study of Circadian Rhythmicity and Photoperiodism in Closely Related Species of Blow Flies: External Coincidence, Maternal Induction, and Diapause at Northern Latitudes

Abstract

This review compares adult locomotor activity rhythms and photoperiodic induction of diapause in 3 common species of blow fly, Calliphora vicina, Lucilia sericata, and Protophormia terraenovae. Activity rhythms were broadly similar in all 3 species, although P. terraenovae is much less sensitive to constant light inducing arrhythmicity. Photoperiodic induction of diapause, on the other hand, varies more widely between species. C. vicina and L. sericata overwinter in a larval diapause induced by autumnal short days (long nights) acting both maternally and directly upon the larvae. P. terraenovae, on the other hand, shows an adult (reproductive) diapause induced by short daylength and low temperature experienced by the larvae. In the Nanda-Hamner protocol, C. vicina shows 3 clear peaks of high diapause incidence in cycle lengths close to 24, 48, and 72 h, without dampening and therefore suggesting a photoperiodic mechanism based on a self-sustained circadian oscillator acting in a clock of the external coincidence type. Entrainment of the locomotor activity rhythm to extended Nanda-Hamner photocycles, as well as to LD cycles close to the limits of the primary range of entrainment, demonstrates that overt circadian rhythmicity may act as ‘hands’ of the otherwise covert photoperiodic system, as suggested by Bünning, nearly 8 decades ago. In 24 h LD cycles, both locomotor activity rhythms and the photoperiodic oscillator are set to constant phase (CT 12) at light-off, so that the photoperiodic clock measures changes in nightlength by the coincidence (or not) of dawn light with a ‘photoinducible phase’ late in the subjective night (at about CT 21.5 h) as photoperiod changes with the seasons. Apparent differences between quantitative and qualitative photoperiodic responses are discussed.

Drosophila ezoana uses morning and evening oscillators to adjust its rhythmic activity to different daylengths but only the morning oscillator to measure night length for photoperiodic responses

“…A series of clever experiments with night-interrupting light-pulses (Nanda and Hamner 1958 ; Bünsow 1960 ) have been performed in aphids, flies and pitcher-plant mosquitos to test the role of the circadian clock in photoperiodic time measurement (Lees 1973 ; Saunders this issue; Bradshaw et al this issue). These indicated that flesh and blow flies rely on the circadian clock (external coincidence) for photoperiodic time measurement (Saunders 2021 ), aphids use an interval timer (‘hourglass’; Lees 1973 ), and the response of pitcher-plant mosquitos depends on their geographical origin (Bradshaw et al this issue). The pitcher-plant mosquito, Wyeomyia smithii , belongs to one of the rare species, in which the photoperiodic response has been systematically investigated in populations living at different latitudes altitudes (Bradshaw et al this issue).…”

“…It may be even independent of the type of photoperiodic response. While Calliphora , Lucilia , Chymomyza and Wyeomyia species diapause as larvae (Enomoto 1982 ; Saunders 2021 ; Bradshaw et al this issue), Sarcophaga diapauses as pupa (Denlinger 1972 ), Protophormia and Drosophila species diapause as adults (Lumme and Lakovaara 1983 ; Numata and Shiga 1995 ), and aphids show a fascinating annual life cycle in which parthenogenetic and sexual reproduction alternate (Colizzi et al this issue).…”

“…In contrast, hymenopterans to which Nasonia vitripennis belongs, lack d-CRY and d-TIM and possess only light-insensitive mammalian CRY (also called m-CRY) that interacts with PER (Kotwica-Rolinska et al 2022 ; Deppisch et al 2023 ). Thus, hymenopterans lack the immediate light response elicited by the degradation of d-TIM by d-CRY, and fittingly, they use internal coincidence to measure daylength (Saunders 2021 ).…”

Time measurement in insect photoperiodism: external and internal coincidence

“…Four rhythmic systems form the basis of the present study. In the first, the rhythm of locomotor activity of the diurnally active adult blow fly Calliphora vicina (Kenny and Saunders 1991 ; Saunders 2021 ) shows the characteristics of rhythmicity in a single insect; this species also passes the winter in a state of larval diapause (Vinogradova and Zinovjeva 1972 ; Saunders 1987 ). The endogenous, circadian nature of the adult fly’s rhythm is revealed upon its transfer from a light–dark cycle into constant darkness (DD), whereupon the periodicity of activity persists (free-runs) with a period τ h differing somewhat from an exact 24 h (Kenny and Saunders 1991 ).…”

Common Ground between Biological Rhythms and Forensics

“…Correlations between the developmental stages and the minimum PMI are well-documented in Calliphoridae that frequently populate a body within hours after death [ 74 ]. The diapause onset of Calliphora vicina orients itself towards length of daily light and dark periods with cycle lengths of 24 h, pointing to a photoperiodic mechanism that could be orchestrated by self-sustained circadian oscillations [ 75 ]. In autumn, for example, short days and long nights compose the characteristic photoperiod that, in turn, induces overwintering in larval diapause in C. vicina [ 76 ].…”