Task-Related Phasing of Circadian Rhythms in Antennal Responsiveness to Odorants and Pheromones in Honeybees

Abstract

The insect antennae receive olfactory information from the environment. In some insects, it has been shown that antennal responsiveness is dynamically regulated by circadian clocks. However, it is unknown how general this phenomenon is and what functions it serves. Circadian regulation in honeybee workers is particularly interesting in this regard because they show natural task-related chronobiological plasticity. Forager bees show strong circadian rhythms in behavior and brain gene expression, whereas nurse bees tend brood around-the-clock and have attenuated circadian rhythms in activity and whole-brain gene expression. Here, we tested the hypothesis that there is task-related plasticity in circadian rhythms of antennal responsiveness to odorants in worker honeybees. We used electroantennogram (EAG) to measure the antennal responsiveness of nurses and foragers to general odorants and pheromones around the day. The capacity to track 10-Hz odorant pulses varied with time of day for both task groups but with different phases. The antennal pulse-tracking capacity was higher during the subjective day for the day-active foragers, whereas it was better during the night for around-the-clock active nurses. The task-related phases of pulse-tracking rhythms were similar for all the tested stimuli. We also found evidence for circadian rhythms in the EAG response magnitude of foragers but not of nurses. To the best of our knowledge, these results provide the first evidence for circadian regulation of antennal olfactory responsiveness and odorant pulse-tracking capacity in bees or any other hymenopteran insect. Importantly, our study shows for the first time that the circadian phase of olfactory responsiveness may be socially regulated.

Nurse honeybee workers tend capped-brood, which does not require feeding, around-the-clock

“…The premise that some processes in around-the-clock active nurses nevertheless show circadian regulation is consistent with a microarray study which showed that some transcripts oscillate in the nurse brain in a different, or even opposite, phase from that of foragers (Rodriguez-Zas et al, 2012). A recent study further suggests that the capacity of the nurse antennae to track pulses of odorant stimuli is higher at night, in almost anti-phase with their peak of locomotor activity rhythms when removed from the hive (Nagari et al, 2017). These findings suggest complex patterns of circadian regulation in nurses: biological processes that are under circadian regulation in foragers may not be under clock regulation in nurses or, alternatively, they may be regulated with phases similar to or different from those of foragers.…”

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

“…expression pattern of clock controlled genes [33,46], some of them involved in foraging associated processes (e.g. olfactory and visual sensitivity [33,47]), and (3.) time-memory [33].…”

Adaptive evolution of olfactory degeneration in recently flightless insects

“…We fixed the stoneflies with adhesive tape and used a razor blade to cut off a 5 mm long section of the distal antennae (the length of the intact antennae was approximately 15 mm). Antennae were mounted with conductive gel (GEL+, Ritex, Germany) on a four-channel silver electrode (64) (Fig. 3A).…”

“…3A). To eliminate between-session variability (e.g., due to humidity or circadian rhythms in antennal responsiveness (64)), the left and right antennae of one full-winged and one wing-reduced stonefly were recorded simultaneously (Fig. 3B).…”