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

Abstract

AbstractDivision 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.

Autoren

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

DOI

10.1038/s42003-023-05273-4

eISSN

2399-3642

Ausgabe der Veröffentlichung

1

Zeitschrift

Communications Biology

Sprache

en

Artikelnummer

1004

Online publication date

2023

Status

Published online

Herausgeber

Springer Science and Business Media LLC

Herausgeber URL

http://dx.doi.org/10.1038/s42003-023-05273-4

Datum der Datenerfassung

2023

Titel

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

Ausgabe der Zeitschrift

6

Datenquelle: Crossref

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.

Addresses

Institute of Organismic and Molecular Evolution, Johannes Gutenberg University Mainz, Mainz, Germany. marcelcaminer@gmail.com.

Autoren

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

DOI

10.1038/s42003-023-05273-4

eISSN

2399-3642

Externe Identifier

PubMed Identifier: 37783732
PubMed Central ID: PMC10545721

Funding acknowledgements

Deutsche Forschungsgemeinschaft: GRK2526/1

Open access

true

ISSN

2399-3642

Ausgabe der Veröffentlichung

1

Zeitschrift

Communications biology

Schlüsselwörter

Animals
Humans
Ants
Receptors, Odorant
Gene Expression Profiling
Gene Expression
Odorants

Sprache

eng

Medium

Electronic

Online publication date

2023

Open access status

Open Access

Paginierung

1004

Datum der Veröffentlichung

2023

Status

Published

Publisher licence

CC BY

Datum der Datenerfassung

2023

Titel

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

Sub types

Research Support, Non-U.S. Gov't
research-article
Journal Article

Ausgabe der Zeitschrift

6

Files

https://europepmc.org/articles/PMC10545721?pdf=render

Datenquelle: Europe PubMed Central

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.

Date of acceptance

2023

Autoren

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

Autoren-URL

https://www.ncbi.nlm.nih.gov/pubmed/37783732

DOI

10.1038/s42003-023-05273-4

eISSN

2399-3642

Externe Identifier

PubMed Central ID: PMC10545721

Ausgabe der Veröffentlichung

1

Zeitschrift

Commun Biol

Schlüsselwörter

Humans
Animals
Ants
Receptors, Odorant
Gene Expression
Gene Expression Profiling
Odorants

Sprache

eng

Country

England

Paginierung

1004

PII

10.1038/s42003-023-05273-4

Datum der Veröffentlichung

2023

Status

Published online

Datum, an dem der Datensatz öffentlich gemacht wurde

2023

Titel

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

Sub types

Journal Article
Research Support, Non-U.S. Gov't

Ausgabe der Zeitschrift

6

Datenquelle: PubMed

Author's licence

CC-BY

Autoren

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

Hosting institution

Universitätsbibliothek Mainz

Sammlungen

DFG-491381577-G

Resource version

Published version

DOI

10.1038/s42003-023-05273-4

File(s) embargoed

false

Open access

true

ISSN

2399-3642

Zeitschrift

Communications biology

Schlüsselwörter

570 Biowissenschaften
570 Life sciences

Sprache

eng

Open access status

Open Access

Paginierung

1004

Datum der Veröffentlichung

2023

Public URL

https://openscience.ub.uni-mainz.de/handle/20.500.12030/9891

Herausgeber

Springer Nature

Datum der Datenerfassung

2024

Datum, an dem der Datensatz öffentlich gemacht wurde

2024

Zugang

Public

Titel

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

Ausgabe der Zeitschrift

6

Files

taskspecific_odorant_receptor-20231218114317249.pdf

Datenquelle: OPENSCIENCE.UB

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

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