Maternity-related plasticity in circadian rhythms of bumble-bee queens

Abstract

Unlike most animals studied so far in which the activity with no circadian rhythms is pathological or linked to deteriorating performance, worker bees and ants naturally care for their sibling brood around the clock with no apparent ill effects. Here, we tested whether bumble-bee queens that care alone for their first batch of offspring are also capable of a similar chronobiological plasticity. We monitored locomotor activity of Bombus terrestris queens at various life cycle stages, and queens for which we manipulated the presence of brood or removed the ovaries. We found that gynes typically emerged from the pupae with no circadian rhythms, but after several days showed robust rhythms that were not affected by mating or diapauses. Colony-founding queens with brood showed attenuated circadian rhythms, irrespective of the presence of ovaries. By contrast, queens that lost their brood switched again to activity with strong circadian rhythms. The discovery that circadian rhythms in bumble-bee queens are regulated by the life cycle and the presence of brood suggests that plasticity in the circadian clock of bees is ancient and related to maternal behaviour or physiology, and is not a derived trait that evolved with the evolution of the worker caste.

Ant circadian activity associated with brood care type

“…From a chronobiological perspective, it is believed that inside-nest workers (i.e. nurses) of social insects had lost their circadian rhythms owing to colony-level selection for rapid growth of broods [5,6,9,12,15]. However, recent research shows that insidenest workers physiologically possess circadian rhythms (i.e.…”

“…Recent studies in honeybees and bumblebees demonstrate that caretakers show arrhythmic activity in the presence of broods [5,6,16], raising the importance of a conditional expression of activity rhythm. Given that colonies have various types of brood that require different types of care (i.e.…”

“…Specifically, interaction with infants or brood brings drastic changes to the activity rhythm of parents or nurses in humans, dolphins and insects [3][4][5][6]. In social insects, nest-mates perform different tasks to achieve a highly organized system as a whole [7].…”

Measuring individual locomotor rhythms in honey bees, paper wasps and similar sized insects

“…The Journal of Experimental Biology (2014) rhythmic behavior in unmated and egg-laying queen bees is dramatically different across colony and isolation conditions (Koeniger and Koeniger, 2000;Harano et al, 2007;Johnson et al, 2010;Eban-Rothschild et al, 2011). Furthermore, it is known that females of both of these paper wasp species can leave their parental nest, develop their reproductive system and become a nest foundress (Ross and Matthews, 1991).…”

“…Both the wide range of biological processes under circadian regulation and the extraordinary plasticity of the circadian network of these organisms potentially represent unique evolutionary challenges and solutions. Despite the potential insight into the functional and evolutionary relevance of circadian rhythms that could be uncovered from studying different social insects, only a few representatives (honey bees and bumble bees) have been studied in depth (Spangler, 1972;Moore and Rankin, 1985;Toma et al, 2000;Eban-Rothschild et al, 2011).…”