Neurogenomic signatures of spatiotemporal memories in time-trained forager honey bees

Abstract

SUMMARYHoney bees can form distinct spatiotemporal memories that allow them to return repeatedly to different food sources at different times of day. Although it is becoming increasingly clear that different behavioral states are associated with different profiles of brain gene expression, it is not known whether this relationship extends to states that are as dynamic and specific as those associated with foraging-related spatiotemporal memories. We tested this hypothesis by training different groups of foragers from the same colony to collect sucrose solution from one of two artificial feeders; each feeder was in a different location and had sucrose available at a different time, either in the morning or afternoon. Bees from both training groups were collected at both the morning and afternoon training times to result in one set of bees that was undergoing stereotypical food anticipatory behavior and another that was inactive for each time of day. Between the two groups with the different spatiotemporal memories, microarray analysis revealed that 1329 genes were differentially expressed in the brains of honey bees. Many of these genes also varied with time of day, time of training or state of food anticipation. Some of these genes are known to be involved in a variety of biological processes, including metabolism and behavior. These results indicate that distinct spatiotemporal foraging memories in honey bees are associated with distinct neurogenomic signatures, and the decomposition of these signatures into sets of genes that are also influenced by time or activity state hints at the modular composition of this complex neurogenomic phenotype. Supplementary material available online at

Comparative brain transcriptomic analyses of scouting across distinct behavioural and ecological contexts in honeybees

“…Perhaps differences in the expression of genes such as odour-binding protein 4 (obp4) reflect some of the differences in the sensory aspects of these two types of scouting. The gene obp4 showed increased brain expression in nest scouts, but was downregulated in food scouts; it also was downregulated in a previous study of scouts [15] and downregulated in active versus inactive foragers [22]. These results suggest differences in responsiveness to olfactory stimuli in the foraging and swarming contexts.…”

“…Three colonies were used to collect food scouts and recruits, and two colonies were used to collect nest scouts and recruits (one colony was used in both food and nest scouting experiments). All bees were foraging age, and collected only in the morning to eliminate possible age and circadian effects on brain gene expression, respectively [22,23].…”

Persistence, reticence, and the management of multiple time memories by forager honey bees

“…Such appointments form the essence of the honey bee time sense: foragers associate the presence of food with both location and time of day and then schedule anticipatory flights to the appropriate location and time on the following day (reviewed in Moore, 2001). Recently, such spatiotemporal memories have been shown to correspond with distinct neurogenomic signatures, as revealed by microarray analyses on time-trained foragers (Naeger et al, 2011). The results of the present study indicate that a forager's appointments do not have to occupy different time slots (i.e.…”

Transcriptomic analysis of instinctive and learned reward-related behaviors in honey bees

“…At the start of each replicate, the colony was moved into a large (20×6×3 m), outdoor, screened enclosure to control the time of food availability (Naeger et al, 2011). Every afternoon at 14:00-17:00 h CST a feeder containing 50% (w/v) sucrose solution was placed in the enclosure at the opposite end of the enclosure from the hive, coinciding with the time that mating flights begin for drones at this locality.…”

“…As with drone mating flights, worker foraging flights also are under the control of an internal clock (Renner, 1957). Transcriptomic analyses revealed that different spatiotemporal foraging memories are associated with distinct patterns of brain gene expression, including genes that regulate circadian rhythms (Naeger et al, 2011). We used these two spatiotemporal flight behaviors in drone and worker honey bees to compare the patterns of gene expression in the brain associated with instinctive and learned behaviors.…”