Task-specific patterns of odorant receptor expression in worker antennae indicates a sensory filter regulating division of labor in ants

Abstract

Division of labor (DOL) is a characteristic trait of insect societies, where tasks are generally performed by groups of specialized individuals. In social insects, young workers perform duties within the safety of the nest (e.g., brood care), while older ones undertake riskier tasks (e.g., foraging for food). This DOL remains dynamic, and workers may switch back and forth when colony needs require. Theoretical models propose that workers differ in their thresholds to take on certain tasks when confronted to task-related stimuli, resulting in variation in their response to such stimuli, task-specialization, and thus DOL. Such models assume that workers differ in how they respond to task-related information rather than in how they perceive such information. Here, we test the hypothesis that DOL rather stems from workers differing in their efficiency to detect task-related stimuli. We used transcriptomics to compare gene expression in the antennae and in the brain between nurses and foragers in the ant Temnothorax longispinosus. We found that seven times as many genes were differentially expressed between the behavioral phenotypes in the antennae compared to the brain. Moreover, nearly half of all odorant receptors genes were differentially expressed, with an overrepresentation of the 9-exon gene subfamily upregulated in the antennae of nurses. These findings indicate that nurses and foragers differ in how they perceive their olfactory environment, and task-related signals. The results of this study support the hypothesis that a sensory filter in the antennae predisposes workers to specialize in specific tasks, and may improve our understanding of DOL in insect societies.

Brain and antennal transcriptomes of host ants reveal potential links between behaviour and the functioning of socially parasitic colonies

“…One candidate we identified among the genes differing between the ants transferred into the original treatment or a colony containing unrelated individuals and/or social parasites was a homologue to the odorant receptor 49b‐like in Temnothorax curvispinosus and most similar to lace_OR205 from the manual annotations of ORs from our focal species (Appendix S1; Jongepier et al, 2022). We additionally used blastn to find the most similar sequence among the ORs previously identified in a closely related species, Temnothorax longispinosus (Jongepier et al, 2022), which has been identified to be from subfamily I3 (Caminer et al, 2023). This subfamily is predicted to have an especially important role since it only occurs once in the genome of many species including L. acervorum according to our BLAST results (Engsontia et al, 2015).…”

“…Other differences between parasitic and non‐parasitic nests, such as a general increase in aggression in parasitic nests, may nevertheless be transcriptionally detectable, for example, in the expression of stress‐related genes. Therefore, we specifically investigated genes related to sensory perception, in particular, odorant receptors, whose expression changes in response to the social environment of ant larvae (Pulliainen et al, 2021) and varies between workers mainly performing tasks inside or outside the nest (Caminer et al, 2023). Odorant receptors, particularly those of the 9‐exon gene family, are known to bind to cuticular hydrocarbons, which play an important role in communication in social insects (Pask et al, 2017; Slone et al, 2017).…”

“…Additionally, by recording the behaviour and spatial position of the ants shortly before sampling, we would like to gain insights into whether and how gene expression in the brain or antenna parallels behavioural changes in the hosts. While many studies focus on transcriptomic changes in the central nervous system, i.e., the brain, which not only processes information from the sensory organs but also directly controls behaviour and thus largely reflects an individual's behavioural phenotype (Robinson et al, 2008), recent work suggests that also the peripheral nervous system, the antennae, play a major role in determining an individual's behavioural phenotype (Caminer et al, 2023; Kennedy et al, 2021). Thus, we decided to sequence both of these tissues to additionally unravel the molecular basis of behaviour.…”

Histone acetyltransferases and external demands influence task switching in Temnothorax ants

“…For example, workers of the ant Temnothorax longispinosus that highly express Vitellogenin-like A ( Vg-like A ) have an increased responsiveness to brood stimuli and display high brood care activity [8,9]. In line with this, half of all 419 odorant receptors are differentially expressed in the antennae of brood carers and foragers in this species, pointing to vastly different sensitivity to chemical cues [10]. Workers can transition multiple times between different behavioural states.…”

“…To address this, we used acorn ant T. longispinosus in which workers specialize in brood care or foraging, and task specialization is linked to age, fertility and distinct transcriptional profiles [8][9][10]24,32]. We manipulated colony demography to induce task switching and coupled these manipulations with the application of inhibitors of p300/CBP histone acetyltransferase (HAT) to disentangle the effects of demand and HAT activity on task specialization.…”