Task-specific odorant receptor expression in worker antennae indicates that sensory filters regulate division of labor in ants

Abstract

Division of labor (DOL) is a characteristic trait of insect societies, where tasks are generally performed by specialized individuals. Inside workers focus on brood or nest care, while others take risks by foraging outside. Theory proposes that workers have different thresholds to perform certain tasks when confronted with task-related stimuli, leading to specialization and consequently DOL. Workers are presumed to vary in their response to task-related cues rather than in how they perceive such information. Here, we test the hypothesis that DOL instead stems from workers varying in their efficiency to detect stimuli of specific tasks. We use transcriptomics to measure mRNA expression levels in the antennae and brain of nurses and foragers of the ant Temnothorax longispinosus. We find seven times as many genes to be differentially expressed between behavioral phenotypes in the antennae compared to the brain. Moreover, half of all odorant receptors are differentially expressed, with an overrepresentation of the 9-exon gene family upregulated in the antennae of nurses. Nurses and foragers thus apparently differ in the perception of their olfactory environment and task-related signals. Our study supports the hypothesis that antennal sensory filters predispose workers to specialize in specific tasks.

Pheromone representation in the ant antennal lobe changes with age

“…Co-expression of odorant receptors and ionotropic receptors in the same OSNs has been documented in flies, mosquitos, and ants, 21 – 23 and our results are consistent with a model where PG b and PG a are each associated with two different receptors responsible for detecting general odorants versus alarm pheromones. The different classes of receptors could be up- or downregulated in opposite directions during aging, 6 leading to higher correlation between the presence of alarm pheromone in the local environment and neural activity in the OSNs innervating PG b and PG a . Odor coding is also shaped by interactions between neurons.…”

“…While it is unknown how these behavioral dynamics are neurally regulated, they could partially be generated by altered salience of behaviorally relevant stimuli. 4 , 6 , 7 Here, we investigated how odor coding in the antennal lobe (AL) changes with age in the context of alarm pheromone communication in the clonal raider ant ( Ooceraea biroi ). 17 Similar to other social insects, 11 , 12 , 16 older ants responded more rapidly to alarm pheromones, the chemical signals for danger.…”

The diverse roles of insulin signaling in insect behavior

“…Thus, two different IIS downstream pathways in two different tissues both contribute to the same phenotypic outcome. Other honey bee species, the wasp Polistes metricus , and the ant Temnothorax longispinosus show similar age- and tissue-related patterns ( 88 , 115 – 117 ), while the bumble bee Bombus terrestris , stingless bee Tetragonisca angustula , and ant Solenopsis invicta show the opposite, at least in terms of age patterns ( 118 – 120 ). The mechanistic implications of these complexities remain unclear.…”