Reappraising social insect behavior through aversive responsiveness and learning.

<h4>Background</h4>The success of social insects can be in part attributed to their division of labor, which has been explained by a response threshold model. This model posits that individuals differ in their response thresholds to task-associated stimuli, so that individuals with lower...

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Autores principales: Edith Roussel, Julie Carcaud, Jean-Christophe Sandoz, Martin Giurfa
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Publicado: Public Library of Science (PLoS) 2009
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spelling oai:doaj.org-article:3a4c37706c47496ea19b654f944a3c982021-11-25T06:17:47ZReappraising social insect behavior through aversive responsiveness and learning.1932-620310.1371/journal.pone.0004197https://doaj.org/article/3a4c37706c47496ea19b654f944a3c982009-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/19142222/pdf/?tool=EBIhttps://doaj.org/toc/1932-6203<h4>Background</h4>The success of social insects can be in part attributed to their division of labor, which has been explained by a response threshold model. This model posits that individuals differ in their response thresholds to task-associated stimuli, so that individuals with lower thresholds specialize in this task. This model is at odds with findings on honeybee behavior as nectar and pollen foragers exhibit different responsiveness to sucrose, with nectar foragers having higher response thresholds to sucrose concentration. Moreover, it has been suggested that sucrose responsiveness correlates with responsiveness to most if not all other stimuli. If this is the case, explaining task specialization and the origins of division of labor on the basis of differences in response thresholds is difficult.<h4>Methodology</h4>To compare responsiveness to stimuli presenting clear-cut differences in hedonic value and behavioral contexts, we measured appetitive and aversive responsiveness in the same bees in the laboratory. We quantified proboscis extension responses to increasing sucrose concentrations and sting extension responses to electric shocks of increasing voltage. We analyzed the relationship between aversive responsiveness and aversive olfactory conditioning of the sting extension reflex, and determined how this relationship relates to division of labor.<h4>Principal findings</h4>Sucrose and shock responsiveness measured in the same bees did not correlate, thus suggesting that they correspond to independent behavioral syndromes, a foraging and a defensive one. Bees which were more responsive to shock learned and memorized better aversive associations. Finally, guards were less responsive than nectar foragers to electric shocks, exhibiting higher tolerance to low voltage shocks. Consequently, foragers, which are more sensitive, were the ones learning and memorizing better in aversive conditioning.<h4>Conclusions</h4>Our results constitute the first integrative study on how aversive responsiveness affects learning, memory and social organization in honeybees. We suggest that parallel behavioral modules (e.g. appetitive, aversive) coexist within each individual bee and determine its tendency to adopt a given task. This conclusion, which is at odds with a simple threshold model, should open new opportunities for exploring the division of labor in social insects.Edith RousselJulie CarcaudJean-Christophe SandozMartin GiurfaPublic Library of Science (PLoS)articleMedicineRScienceQENPLoS ONE, Vol 4, Iss 1, p e4197 (2009)
institution DOAJ
collection DOAJ
language EN
topic Medicine
R
Science
Q
spellingShingle Medicine
R
Science
Q
Edith Roussel
Julie Carcaud
Jean-Christophe Sandoz
Martin Giurfa
Reappraising social insect behavior through aversive responsiveness and learning.
description <h4>Background</h4>The success of social insects can be in part attributed to their division of labor, which has been explained by a response threshold model. This model posits that individuals differ in their response thresholds to task-associated stimuli, so that individuals with lower thresholds specialize in this task. This model is at odds with findings on honeybee behavior as nectar and pollen foragers exhibit different responsiveness to sucrose, with nectar foragers having higher response thresholds to sucrose concentration. Moreover, it has been suggested that sucrose responsiveness correlates with responsiveness to most if not all other stimuli. If this is the case, explaining task specialization and the origins of division of labor on the basis of differences in response thresholds is difficult.<h4>Methodology</h4>To compare responsiveness to stimuli presenting clear-cut differences in hedonic value and behavioral contexts, we measured appetitive and aversive responsiveness in the same bees in the laboratory. We quantified proboscis extension responses to increasing sucrose concentrations and sting extension responses to electric shocks of increasing voltage. We analyzed the relationship between aversive responsiveness and aversive olfactory conditioning of the sting extension reflex, and determined how this relationship relates to division of labor.<h4>Principal findings</h4>Sucrose and shock responsiveness measured in the same bees did not correlate, thus suggesting that they correspond to independent behavioral syndromes, a foraging and a defensive one. Bees which were more responsive to shock learned and memorized better aversive associations. Finally, guards were less responsive than nectar foragers to electric shocks, exhibiting higher tolerance to low voltage shocks. Consequently, foragers, which are more sensitive, were the ones learning and memorizing better in aversive conditioning.<h4>Conclusions</h4>Our results constitute the first integrative study on how aversive responsiveness affects learning, memory and social organization in honeybees. We suggest that parallel behavioral modules (e.g. appetitive, aversive) coexist within each individual bee and determine its tendency to adopt a given task. This conclusion, which is at odds with a simple threshold model, should open new opportunities for exploring the division of labor in social insects.
format article
author Edith Roussel
Julie Carcaud
Jean-Christophe Sandoz
Martin Giurfa
author_facet Edith Roussel
Julie Carcaud
Jean-Christophe Sandoz
Martin Giurfa
author_sort Edith Roussel
title Reappraising social insect behavior through aversive responsiveness and learning.
title_short Reappraising social insect behavior through aversive responsiveness and learning.
title_full Reappraising social insect behavior through aversive responsiveness and learning.
title_fullStr Reappraising social insect behavior through aversive responsiveness and learning.
title_full_unstemmed Reappraising social insect behavior through aversive responsiveness and learning.
title_sort reappraising social insect behavior through aversive responsiveness and learning.
publisher Public Library of Science (PLoS)
publishDate 2009
url https://doaj.org/article/3a4c37706c47496ea19b654f944a3c98
work_keys_str_mv AT edithroussel reappraisingsocialinsectbehaviorthroughaversiveresponsivenessandlearning
AT juliecarcaud reappraisingsocialinsectbehaviorthroughaversiveresponsivenessandlearning
AT jeanchristophesandoz reappraisingsocialinsectbehaviorthroughaversiveresponsivenessandlearning
AT martingiurfa reappraisingsocialinsectbehaviorthroughaversiveresponsivenessandlearning
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