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Rapid decision-making with side-specific perceptual discrimination in ants.

Stroeymeyt N, Guerrieri FJ, van Zweden JS, d'Ettorre P - PLoS ONE (2010)

Bottom Line: Our results strongly suggest that first-order olfactory processing centers (up to the antennal lobes) are likely to play a key role in ant nestmate recognition.We hypothesize that the coarse level of discrimination achieved in the antennal lobes early in odor processing provides enough information to determine appropriate behavioral responses towards non-nestmates.This asks for a reappraisal of the mechanisms underlying social recognition in insects.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Centre for Social Evolution, University of Copenhagen, Copenhagen, Denmark. Nathalie.Stroeymeyt@bristol.ac.uk

ABSTRACT

Background: Timely decision making is crucial for survival and reproduction. Organisms often face a speed-accuracy trade-off, as fully informed, accurate decisions require time-consuming gathering and treatment of information. Optimal strategies for decision-making should therefore vary depending on the context. In mammals, there is mounting evidence that multiple systems of perceptual discrimination based on different neural circuits emphasize either fast responses or accurate treatment of stimuli depending on the context.

Methodology/principal findings: We used the ant Camponotus aethiops to test the prediction that fast information processing achieved through direct neural pathways should be favored in situations where quick reactions are adaptive. Social insects discriminate readily between harmless group-members and dangerous strangers using easily accessible cuticular hydrocarbons as nestmate recognition cues. We show that i) tethered ants display rapid aggressive reactions upon presentation of non-nestmate odor (120 to 160 ms); ii) ants' aggressiveness towards non-nestmates can be specifically reduced by exposure to non-nestmate odor only, showing that social interactions are not required to alter responses towards non-nestmates; iii) decision-making by ants does not require information transfer between brain hemispheres, but relies on side-specific decision rules.

Conclusions/significance: Our results strongly suggest that first-order olfactory processing centers (up to the antennal lobes) are likely to play a key role in ant nestmate recognition. We hypothesize that the coarse level of discrimination achieved in the antennal lobes early in odor processing provides enough information to determine appropriate behavioral responses towards non-nestmates. This asks for a reappraisal of the mechanisms underlying social recognition in insects.

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Effect of exposure to alien colony odor on nestmate recognition.(A) Experimental design. Workers from colony X were exposed to the odor of either nestmates (XX) or non-nestmates from colony Y (XY), either inside sub-colonies during 24 hours (experiment 1) or directly on their antennae during 18 hours (experiment 2). Aggression tests between treated workers and anaesthetized target workers from colonies X, Y or unrelated alien Z were performed immediately after exposure as indicated by the arrows. (B) Restrained worker in the antennal exposure device. The picture shows CHC-coated glass capillaries positioned around the worker's antennae. (C, D) Aggression level of treated workers towards targets from colonies X (yellow bars), Y (blue bars) and Z (black bars) in experiments 1 (C) and 2 (D). Columns and error bars indicate mean and standard error of aggression indices respectively. Different letters indicate significant differences between categories (mixed-effects model with least square means post-hoc comparisons, P<0.05). XY workers were significantly less aggressive towards non-nestmates from colony Y than XX workers (XY–Y vs. XX–Y: P<0.0001 in both experiments). However, treatments did not influence aggressiveness towards nestmates (XX–X vs. XY–X, experiment 1: P = 0.808; experiment 2: P = 0.837) or non-nestmates from colony Z (XX–Z vs. XY–Z, experiment 1: P = 0. 322; experiment 2: P = 0. 416).
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pone-0012377-g001: Effect of exposure to alien colony odor on nestmate recognition.(A) Experimental design. Workers from colony X were exposed to the odor of either nestmates (XX) or non-nestmates from colony Y (XY), either inside sub-colonies during 24 hours (experiment 1) or directly on their antennae during 18 hours (experiment 2). Aggression tests between treated workers and anaesthetized target workers from colonies X, Y or unrelated alien Z were performed immediately after exposure as indicated by the arrows. (B) Restrained worker in the antennal exposure device. The picture shows CHC-coated glass capillaries positioned around the worker's antennae. (C, D) Aggression level of treated workers towards targets from colonies X (yellow bars), Y (blue bars) and Z (black bars) in experiments 1 (C) and 2 (D). Columns and error bars indicate mean and standard error of aggression indices respectively. Different letters indicate significant differences between categories (mixed-effects model with least square means post-hoc comparisons, P<0.05). XY workers were significantly less aggressive towards non-nestmates from colony Y than XX workers (XY–Y vs. XX–Y: P<0.0001 in both experiments). However, treatments did not influence aggressiveness towards nestmates (XX–X vs. XY–X, experiment 1: P = 0.808; experiment 2: P = 0.837) or non-nestmates from colony Z (XX–Z vs. XY–Z, experiment 1: P = 0. 322; experiment 2: P = 0. 416).

Mentions: We exposed workers to colony-specific odors by introducing CHC-coated microscope slides into sub-colonies for 24 hours (experiment 1) or by positioning CHC-coated glass capillaries over the antennae of individual workers for 18 hours (experiment 2; Figure 1A, B). These two procedures gave similar results (Figure 1C, D): workers exposed to CHCs of an alien colony became significantly less aggressive towards freshly killed non-nestmates from that colony, as compared to workers that were exposed to nestmate CHCs (GLMM, least square means comparisons: p<0.0001). Test workers had therefore familiarized themselves with non-nestmate odor upon prolonged exposure to that stimulus. This familiarization process was specific, as workers exposed to non-nestmate CHCs from a given colony did not lower their aggressiveness towards non-nestmates from a different, unfamiliar colony.


Rapid decision-making with side-specific perceptual discrimination in ants.

Stroeymeyt N, Guerrieri FJ, van Zweden JS, d'Ettorre P - PLoS ONE (2010)

Effect of exposure to alien colony odor on nestmate recognition.(A) Experimental design. Workers from colony X were exposed to the odor of either nestmates (XX) or non-nestmates from colony Y (XY), either inside sub-colonies during 24 hours (experiment 1) or directly on their antennae during 18 hours (experiment 2). Aggression tests between treated workers and anaesthetized target workers from colonies X, Y or unrelated alien Z were performed immediately after exposure as indicated by the arrows. (B) Restrained worker in the antennal exposure device. The picture shows CHC-coated glass capillaries positioned around the worker's antennae. (C, D) Aggression level of treated workers towards targets from colonies X (yellow bars), Y (blue bars) and Z (black bars) in experiments 1 (C) and 2 (D). Columns and error bars indicate mean and standard error of aggression indices respectively. Different letters indicate significant differences between categories (mixed-effects model with least square means post-hoc comparisons, P<0.05). XY workers were significantly less aggressive towards non-nestmates from colony Y than XX workers (XY–Y vs. XX–Y: P<0.0001 in both experiments). However, treatments did not influence aggressiveness towards nestmates (XX–X vs. XY–X, experiment 1: P = 0.808; experiment 2: P = 0.837) or non-nestmates from colony Z (XX–Z vs. XY–Z, experiment 1: P = 0. 322; experiment 2: P = 0. 416).
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2927537&req=5

pone-0012377-g001: Effect of exposure to alien colony odor on nestmate recognition.(A) Experimental design. Workers from colony X were exposed to the odor of either nestmates (XX) or non-nestmates from colony Y (XY), either inside sub-colonies during 24 hours (experiment 1) or directly on their antennae during 18 hours (experiment 2). Aggression tests between treated workers and anaesthetized target workers from colonies X, Y or unrelated alien Z were performed immediately after exposure as indicated by the arrows. (B) Restrained worker in the antennal exposure device. The picture shows CHC-coated glass capillaries positioned around the worker's antennae. (C, D) Aggression level of treated workers towards targets from colonies X (yellow bars), Y (blue bars) and Z (black bars) in experiments 1 (C) and 2 (D). Columns and error bars indicate mean and standard error of aggression indices respectively. Different letters indicate significant differences between categories (mixed-effects model with least square means post-hoc comparisons, P<0.05). XY workers were significantly less aggressive towards non-nestmates from colony Y than XX workers (XY–Y vs. XX–Y: P<0.0001 in both experiments). However, treatments did not influence aggressiveness towards nestmates (XX–X vs. XY–X, experiment 1: P = 0.808; experiment 2: P = 0.837) or non-nestmates from colony Z (XX–Z vs. XY–Z, experiment 1: P = 0. 322; experiment 2: P = 0. 416).
Mentions: We exposed workers to colony-specific odors by introducing CHC-coated microscope slides into sub-colonies for 24 hours (experiment 1) or by positioning CHC-coated glass capillaries over the antennae of individual workers for 18 hours (experiment 2; Figure 1A, B). These two procedures gave similar results (Figure 1C, D): workers exposed to CHCs of an alien colony became significantly less aggressive towards freshly killed non-nestmates from that colony, as compared to workers that were exposed to nestmate CHCs (GLMM, least square means comparisons: p<0.0001). Test workers had therefore familiarized themselves with non-nestmate odor upon prolonged exposure to that stimulus. This familiarization process was specific, as workers exposed to non-nestmate CHCs from a given colony did not lower their aggressiveness towards non-nestmates from a different, unfamiliar colony.

Bottom Line: Our results strongly suggest that first-order olfactory processing centers (up to the antennal lobes) are likely to play a key role in ant nestmate recognition.We hypothesize that the coarse level of discrimination achieved in the antennal lobes early in odor processing provides enough information to determine appropriate behavioral responses towards non-nestmates.This asks for a reappraisal of the mechanisms underlying social recognition in insects.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Centre for Social Evolution, University of Copenhagen, Copenhagen, Denmark. Nathalie.Stroeymeyt@bristol.ac.uk

ABSTRACT

Background: Timely decision making is crucial for survival and reproduction. Organisms often face a speed-accuracy trade-off, as fully informed, accurate decisions require time-consuming gathering and treatment of information. Optimal strategies for decision-making should therefore vary depending on the context. In mammals, there is mounting evidence that multiple systems of perceptual discrimination based on different neural circuits emphasize either fast responses or accurate treatment of stimuli depending on the context.

Methodology/principal findings: We used the ant Camponotus aethiops to test the prediction that fast information processing achieved through direct neural pathways should be favored in situations where quick reactions are adaptive. Social insects discriminate readily between harmless group-members and dangerous strangers using easily accessible cuticular hydrocarbons as nestmate recognition cues. We show that i) tethered ants display rapid aggressive reactions upon presentation of non-nestmate odor (120 to 160 ms); ii) ants' aggressiveness towards non-nestmates can be specifically reduced by exposure to non-nestmate odor only, showing that social interactions are not required to alter responses towards non-nestmates; iii) decision-making by ants does not require information transfer between brain hemispheres, but relies on side-specific decision rules.

Conclusions/significance: Our results strongly suggest that first-order olfactory processing centers (up to the antennal lobes) are likely to play a key role in ant nestmate recognition. We hypothesize that the coarse level of discrimination achieved in the antennal lobes early in odor processing provides enough information to determine appropriate behavioral responses towards non-nestmates. This asks for a reappraisal of the mechanisms underlying social recognition in insects.

Show MeSH
Related in: MedlinePlus