Neuronal circadian clock protein oscillations are similar in behaviourally rhythmic forager honeybees and in arrhythmic nurses

Abstract

Internal clocks driving rhythms of about a day (circadian) are ubiquitous in animals, allowing them to anticipate environmental changes. Genetic or environmental disturbances to circadian clocks or the rhythms they produce are commonly associated with illness, compromised performance or reduced survival. Nevertheless, some animals including Arctic mammals, open sea fish and social insects such as honeybees are active around-the-clock with no apparent ill effects. The mechanisms allowing this remarkable natural plasticity are unknown. We generated and validated a new and specific antibody against the clock protein PERIOD of the honeybee Apis mellifera (amPER) and used it to characterize the circadian network in the honeybee brain. We found many similarities to Drosophila melanogaster and other insects, suggesting common anatomical organization principles in the insect clock that have not been appreciated before. Time course analyses revealed strong daily oscillations in amPER levels in foragers, which show circadian rhythms, and also in nurses that do not, although the latter have attenuated oscillations in brain mRNA clock gene levels. The oscillations in nurses show that activity can be uncoupled from the circadian network and support the hypothesis that a ticking circadian clock is essential even in around-the-clock active animals in a constant physical environment.

Two sides of a coin: ecological and chronobiological perspectives of timing in the wild

“…In the absence of circadian behaviour, some pacemakers nevertheless continue to tick in the brains of the bees, even under the tightly regulated physical environment of the hive. This observation underlines a high degree of plasticity in the circadian system [81][82][83].…”

“…This plasticity is regulated by contact with the brood (reviewed in [72,113]). Gene expression studies have shown that shifts to brood care are associated with attenuation in the cyclic expression of whole brain mRNA levels of clock genes such as Period, Cryptochrome-m, Cycle and Clockwork Orange, but not in the abundance of PERIOD protein in pacemaker neurons, suggesting complex socially modulated reorganization of the circadian system of social bees [81,83,114]. Shifts also occur seasonally, for example, to nocturnality of diurnal birds during the migration season, which can be triggered endogenously by circannual rhythms.…”

Time-restricted foraging under natural light/dark condition shifts the molecular clock in the honey bee,Apis mellifera

“…Thus, we cannot exclude the possibility that these changes occurred in brain cells, e.g. glia, that do not strictly belong to the neuron populations representing the central insect brain clock [36]. On the other hand, studies in Drosophila and honey bees suggest that behavioral activity rhythms are regulated by the central brain clock [36–39].…”

Neonicotinoids Disrupt Circadian Rhythms and Sleep in Honey Bees

“…Honey bees are highly dependent on circadian clocks to regulate critical behaviors, such as foraging orientation and navigation, time-memory for food sources, sleep, and learning/ memory processes [5][6][7][8] . Circadian clock neurons in Drosophila receive light input through cholinergic signaling 9 , and honey bees possess homologous clusters of putative clock neurons 10,11 , thus honey bee clock neurons are potential targets for neonicotinoid effects. Sublethal doses of neonicotinoid pesticides have been shown to disrupt navigation by forager honey bees 12,13 .…”