Evidence map›Paper›PMID 19706434›Full record

ArticleProceedings of the National Academy of Sciences of the United States of America2009

Honey bee aggression supports a link between gene regulation and behavioral evolution.

Cédric Alaux, Saurabh Sinha, Linda Hasadsri, Greg J Hunt, Ernesto Guzmán-Novoa, Gloria DeGrandi-Hoffman, José Luis Uribe-Rubio, Bruce R Southey, Sandra Rodriguez-Zas, Gene E Robinson

Open access · greenAbstract read
In one paragraph

Article in Proceedings of the National Academy of Sciences of the United States of America, 2009. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 124 papers.

0numbers the graph read from it
0cells of the map it votes in
124citing papers in PubMed
9.8field-weighted citation impact, top 2% of its field
1 · What the graph read from it

What it found

Each row is one number read from the abstract, on the scale the paper reported it, with its interval. Left of the dashed line favours the treatment, right favours the comparator. Under each row is the sentence it came from. New to these charts? A ten-minute tutorial.

The abstract states no effect estimate the extractor could read, or names no intervention and outcome on the map, so this paper lights no cell and moves no belief. It is still indexed, cited and linked below.

2 · The registry

The trial behind it

Trials whose registry record cites this paper, or whose number appears in the abstract. A trial that started after this paper was published is citing it as background, not reporting it.

Neither the registry nor the abstract names a trial number. If this is a trial report, that itself is worth knowing.

3 · Its place in the literature

Who cites it

124 citing papers in PubMed, 279 citations in OpenAlex.

  1. Article
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  6. Division of labour during honeybee colony defence: poetic and scientific views.Philosophical transactions of the Royal Society of London. Series B, Biological sciences · 2025
    Review
  7. Division of labour in colony defence in a clonal ant.Philosophical transactions of the Royal Society of London. Series B, Biological sciences · 2025
    Article
  8. Article
  9. Article
  10. Review
  11. Article
  12. Review
  13. Article
  14. Article
  15. Honey Bee Colonies (Insects · 2023
    Article
  16. Article
  17. Article
  18. Distinct gene regulatory signatures of dominance rank and social bond strength in wild baboons.Philosophical transactions of the Royal Society of London. Series B, Biological sciences · 2022
    Article
  19. Article
  20. Article

64 more citing papers are in PubMed but not listed here.

4 · The record

Corrections and comments

PubMed lists nothing against this paper. Absence here is not a guarantee, only a check that was made.

5 · Who and what money

Authors and funding

10 authors at 6 institutions in 6 countries.

Cédric AlauxDepartment of Entomology, University of Illinois, Urbana, IL 61801, USA.
Saurabh Sinha
Linda Hasadsri
Greg J Hunt
Ernesto Guzmán-Novoa
Gloria DeGrandi-Hoffman
José Luis Uribe-Rubio
Bruce R Southey
Sandra Rodriguez-Zas
Gene E Robinson
University of Illinois Urbana-Champaign · USCarl Hayden Bee Research Center · USCenter for Genomic Science · ITInstituto Nacional de Investigaciones Forestales Agrícolas y Pecuarias · MXPurdue University West Lafayette · USUniversity of Guelph · CA

Funding

The UIUC Neuroproteomics Center on Cell-Cell SignalingP30DA018310 · NIDA · UNIVERSITY OF ILLINOIS URBANA-CHAMPAIGN · PI Elena V Romanova · 2004 to 2026
$24.9M
Pheromone regulation of gene expression in the brainR01DC006395 · NIDCD · UNIVERSITY OF ILLINOIS URBANA-CHAMPAIGN · PI ROBINSON, GENE E · 2004 to 2007
$1.1M
Mathematic descriptions - multifactorial gene expressionR01GM068946 · NIGMS · UNIVERSITY OF ILLINOIS URBANA-CHAMPAIGN · PI RODRIGUEZ ZAS, SANDRA L · 2003 to 2006
$1.1M
NIDA NIH HHS P30 DA018310NIDCD NIH HHS DC 006395NIDCD NIH HHS R01 DC006395NIGMS NIH HHS 5 R01 GM068946NIGMS NIH HHS R01 GM068946
6 · The paper itself

Abstract

A prominent theory states that animal phenotypes arise by evolutionary changes in gene regulation, but the extent to which this theory holds true for behavioral evolution is not known. Because "nature and nurture" are now understood to involve hereditary and environmental influences on gene expression, we studied whether environmental influences on a behavioral phenotype, i.e., aggression, could have evolved into inherited differences via changes in gene expression. Here, with microarray analysis of honey bees, we show that aggression-related genes with inherited patterns of brain expression are also environmentally regulated. There were expression differences in the brain for hundreds of genes between the highly aggressive Africanized honey bee compared with European honey bee (EHB) subspecies. Similar results were obtained for EHB in response to exposure to alarm pheromone (which provokes aggression) and when comparing old and young bees (aggressive tendencies increase with age). There was significant overlap of the gene lists generated from these three microarray experiments. Moreover, there was statistical enrichment of several of the same cis regulatory motifs in promoters of genes on all three gene lists. Aggression shows a remarkably robust brain molecular signature regardless of whether it occurs because of inherited, age-related, or environmental (social) factors. It appears that one element in the evolution of different degrees of aggressive behavior in honey bees involved changes in regulation of genes that mediate the response to alarm pheromone.

Indexed as

AggressionBiological EvolutionGene Expression RegulationAnimalsBeesBehavior, AnimalBrainEnzymesMexicoMitochondrial ProteinsOligonucleotide Array Sequence AnalysisPrincipal Component AnalysisRegulatory Elements, TranscriptionalSpecies SpecificityEnzymesMitochondrial Proteins

Identifiers

PMID19706434
PMCPMC2730357
OpenAlexW2132083335

What OpenQuestion holds

Textmetadata
Read underepoch 390

Registered trials

None linked

Read under generation 80e0d062 · epoch 390. Bibliography from PubMed, PubMed Central and OpenAlex; grants from NIH RePORTER; trial links from ClinicalTrials.gov; estimates, votes and beliefs from the OpenQuestion graph.