Behavior Genetics

, Volume 46, Issue 2, pp 242–251 | Cite as

Association of Amine-Receptor DNA Sequence Variants with Associative Learning in the Honeybee

  • Malgorzata Lagisz
  • Alison R. Mercer
  • Charlotte de Mouzon
  • Luana L. S. Santos
  • Shinichi Nakagawa
Original Research


Octopamine- and dopamine-based neuromodulatory systems play a critical role in learning and learning-related behaviour in insects. To further our understanding of these systems and resulting phenotypes, we quantified DNA sequence variations at six loci coding octopamine—and dopamine-receptors and their association with aversive and appetitive learning traits in a population of honeybees. We identified 79 polymorphic sequence markers (mostly SNPs and a few insertions/deletions) located within or close to six candidate genes. Intriguingly, we found that levels of sequence variation in the protein-coding regions studied were low, indicating that sequence variation in the coding regions of receptor genes critical to learning and memory is strongly selected against. Non-coding and upstream regions of the same genes, however, were less conserved and sequence variations in these regions were weakly associated with between-individual differences in learning-related traits. While these associations do not directly imply a specific molecular mechanism, they suggest that the cross-talk between dopamine and octopamine signalling pathways may influence olfactory learning and memory in the honeybee.


Olfactory conditioning Learning Memory Candidate genes Polymorphism Pleiotropy 



We thank Jamie McQuillan, David Jarriault, Kim Garrett and Murray McKenzie for technical assistance with the project. LLSS was supported by a University of Otago Research Grant.

Compliance with ethical standards

Conflicts of interest

Malgorzata Lagisz, Alison R. Mercer, Charlotte de Mouzon, Luana L. S. Santos and Shinichi Nakagawa declare that they have no conflicts of interest.

Human and animal rights and informed consent

This article does not contain any studies with human participants performed by any of the authors. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. For this type of study formal consent is not required.

Supplementary material

10519_2015_9749_MOESM1_ESM.docx (2.3 mb)
Supplementary material 1 (DOCX 2398 kb)


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Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Malgorzata Lagisz
    • 1
    • 2
  • Alison R. Mercer
    • 1
  • Charlotte de Mouzon
    • 1
  • Luana L. S. Santos
    • 1
  • Shinichi Nakagawa
    • 1
    • 2
  1. 1.Department of ZoologyUniversity of OtagoOtago, DunedinNew Zealand
  2. 2.School of BEES, Evolution & Ecology Research CentreThe University of New South Wales, UNSW SydneySydneyAustralia

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