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

Communications Biology · 6 authors, 4 centres

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Transcriptomic analysis of nurse and forager antennae and brains in Temnothorax longispinosus ants found that half of all odorant receptor genes are differentially expressed between task groups in antennae, suggesting task-specific sensory filters underlie division of labor.

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This preclinical study analyzed brain and antenna transcriptomes of nurses and foragers in the ant Temnothorax longispinosus to test whether task-specific sensory filtering contributes to division of labor. The authors found nearly seven times as many differentially expressed genes in antennae as in the brain, with half of all odorant receptor (OR) genes differentially expressed between task groups in the antennae. Nurses upregulated genes from the 9-exon OR subfamily, which is implicated in social communication and detection of cuticular hydrocarbons, while foragers upregulated a greater number of OR subfamilies (19 vs. 3), potentially reflecting adaptation to a more chemically diverse external environment. Multiple genes in biogenic pathways were also differentially expressed, potentially fine-tuning odorant filter sensitivity. A key limitation is that age was not directly measured, though previous work on this species indicates behavioral specialization is more strongly associated with gene expression than age. These findings support the hypothesis that dynamic, task-specific sensory filters in peripheral organs contribute to behavioral specialization in social insect workers.

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other

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preclinical research

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ORIGINAL PAPER

PMC10545721

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

Communications Biology

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ABSTRACT

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. Subject terms: Social evolution, Behavioural ecology

CITATION EXPORT

Marcel A Caminer, Romain Libbrecht, Megha Majoe et al.. Task-specific odorant receptor expression in worker antennae indicates that sensory filters regulate division of labor in ants. Communications Biology. (2023). https://doi.org/10.1038/s42003-023-05273-4

AUTHORS

6 · 4 CENTRES

Marcel A Caminer, Romain Libbrecht, Megha Majoe, David V Ho, Peter Baumann, Susanne Foitzik

1Institute of Organismic and Molecular Evolution, Johannes Gutenberg University Mainz, Mainz, Germany
2Institut de Recherche sur la Biologie de l’Insecte, UMR 7261, CNRS, University of Tours, Tours, France
3Institute of Developmental and Neurobiology, Johannes Gutenberg University Mainz, Mainz, Germany
4Institute of Molecular Biology, Mainz, Germany

Marcel A Caminer, Romain Libbrecht, Megha Majoe et al.. Task-specific odorant receptor expression in worker antennae indicates that sensory filters regulate division of labor in ants. Communications Biology. (2023). https://doi.org/10.1038/s42003-023-05273-4