EVOLBEE: cognition, reproduction and adaptation in the honeybee



Research aims

Bees are a fruitful research model and a prominent agricultural agent. Although numerous studies have been devoted to these insects in the past, a large part of their behavior and of their evolutionary history are still unknown. Our general objective is to provide a better understanding of the rules underlying bees’ adaptation to their environment and to determine the genetic and nervous bases of their behavior by bringing an evolutionary perspective to these studies. Bees show elaborate cognitive capacities, which could be linked to the adaptation of their central nervous system to the constraints related to foraging in a highly complex environment and to their eusocial biology.

To understand the importance of these adaptations and of their potential evolutionary origin, we study the perception, learning and memory capacities of the bees at both individual and colony levels. We are also interested in pheromonal communication between sexuals, from individual to population levels (male congregations). This research aims to understand potential speciation mechanisms (sexual isolation) between the different species of the genus Apis and between subspecies of A. mellifera. In parallel, studies on the evolutionary history of the species with neutral markers are pursued focusing on the reproducing function of a population of bees. Finally, we carry out research aimed at understanding the risks of and protecting bees against potential dangers such as pesticides or an invasive species, the yellow-legged hornet.

  [to our publications]

Team members

Researchers and Lecturers

  • Gérard Arnold, Emeritus CNRS Research Director. Honeybee behaviour: impact of the invasive hornet Vespa velutina on honeybees and the ecosystem; the honeybee as a bioindicator.
  • Lionel Garnery, Lecturer, University of Versailles Saint-Quentin en Yvelines. Evolutionary history of honeybee species, phylogeography, molecular evolution, conservation of genetic and ecoethological diversity in honeybees.
  • Jean-Christophe Sandoz, CNRS Research Director, Team Leader. Olfactory and visual perception and learning in the honeybee. Sensory and neural circuits involved in pheromone perception in different honeybee species and subspecies. Techniques: in vivo calcium imaging, neuroanatomy, behaviour (appetitive and aversive conditioning, orientation).

Engineers et Technicians

  • Damien Delalande, CNRS Engineer (on contract). Ecoethological and genetic survey of honeybee preservation areas.
  • Virginie Larcher, CNRS Assistant Engineer. Neuroanatomy et neurophysiology in Hymenoptera.
  • Hélène Legout, CNRS Assistant Engineer. Molecular biology, characterization of honeybee genetic diversity.


PhD students

  • Hanna Cholé, PhD Student. Social learning in honeybees
  • Julia Mariette, PhD Student. Sex communication olfactory receptors in honeybees.

Master students

  • Amélie Noël, Master2. Sex communication olfactory receptors in honeybees.


  • Mohamed Alburaki, PhD student, Analysis of honeybee genetic diversity in Syrian honeybee (A. m. syriaca) populations.
  • Mariangela Arca, PhD student. Genetic characterization and behavioural study of an invasive hornet species in France: Vespa velutina.
  • Bénédicte Bertrand, PhD student. Role of drones in the genetic diversity of honeybee populations.
  • Andreas Brandstaetter, NeRF Postdoctoral fellow. Evolution of pheromonal communication in the genus Apis.
  • Julie Carcaud, PhD student. Function of the dual olfactory system of honeybees: behavioural and neurophysiological approaches.
  • Antoine Couto, Phd student, then postdoc. Behaviour and neuroanatomy of the invasive hornet Vespa velutina.
  • Joey Dimaggio, Master2. Spatial and temporal dynamics of infectious agents in honeybees.
  • Nicholas Henderson, Master 2 Research student. Olfactory mixture learning in honeybees.
  • Kevin Fradin, PhD Student. Behavioural study of olfactory learning in the invasive hornet Vespa velutina.
  • Pierre Junca, PhD Student. Behavioural and genetic study of aversive and appetitive learning in honeybees.
  • Justine Leloup, Master 2 Research student. Bimodal learning in honeybees.
  • Yves Loublier, Research Engineer. Palynology.
  • Ana-Carolina Roselino, FAPESP postdoctoral fellow. Neuroanatomy of the stingless bee brain.
  • Michel Solignac, Professor at University Paris XI, Honeybee genetics.
  • Marie-Anne Wycke, Master 2 Research student. Learning of olfactory mixtures in honeybees.

 Team Publications


  • Brand, P., Larcher, V., Couto, A., Sandoz J.C.*, Ramirez, S.* (2018). Sexual dimorphism in visual and olfactory brain centers in the perfume-collecting orchid bee Euglossa dilemma (Hymenoptera, Apidae). Journal of Comparative Neurology (in press)
  • Carcaud, J., Giurfa, M., Sandoz J.C. (2018). Differential processing by two olfactory subsystems in the honeybee brain. Neuroscience, 378, 33-48.
  • Mancini, N., Giurfa, M., Sandoz J.C., Avarguès-Weber, A. (2018). Aminergic neuromodulation of associative visual learning in harnessed honey bees. Neurobiology of Learning and Memory (in press).
  • Monceau, K., Arca, M., Leprêtre, L., Bonnard, O., Arnold, G., Thiéry, D. (2018). How Apis mellifera behaves with its invasive hornet predator Vespa velutina. Journal of Insect Behavior, 31, 1-11.
  • Oulhaci, C.M., Denis, B., Kilani-Morakchi, S., Sandoz, J.C., Kaiser-Arnaud, L., Joly, D., Aribi, N. (2018). Azadirachtin effects on mating success, gametic abnormalities and progeny survival in Drosophila melanogaster (Diptera). Pest Management Science, 74, 174-180.


  • Aribi, N., Oulhaci, C.M., Kilani-Morakchi, S., Sandoz, J.C., Kaiser-Arnaud, L., Denis, B., Joly, D. (2017). Azadirachtin impact on mate choice, female sexual receptivity and male activity in Drosophila melanogaster (Diptera: Drosophilidae). Pesticide Biochemistry and Physiology, 143, 95-101.
  • Bastin, F., Cholé, H., Lafon, G., Sandoz, J.C. (2017). Virgin queen attraction toward males in honey bees. Scientific Reports, 7(1): 6293, 1-11.
  • Bastin, F., Savarit, F., Lafon, G., Sandoz, J.C. (2017). Age-specific olfactory attraction between Western honey bee drones (Apis mellifera) and its chemical basis. PLoS ONE, 12(10), e0185949, 1-22.
  • Buatois, A., Pichot, C., Schultheiss, P., Sandoz, J.C., Lazzari, C.R., Chittka, L., Avarguès-Weber, A., Giurfa, M. (2017). Associative visual learning by tethered bees in a controlled visual environment. Scientific Reports, 7(1), 12903, 1-19.
  • Chávez-Galarza, J., Garnery, L., Henriques, D., Neves, C.J., Loucif-Ayad, W., Jonhston, J.S., Pinto, M.A. (2017). Mitochondrial DNA variation of Apis mellifera iberiensis: further insights from a large-scale study using sequence data of the tRNAleu-cox2 intergenic region. Apidologie, 48, 533-544.
  • Couto, A., Mitra, A., Thiéry, D., Marion-Poll, F., Sandoz, J.C. (2017). Hornets have it: a conserved olfactory subsystem for social recognition in Hymenoptera? Frontiers in Neuroanatomy, 11: 48, 1-12.
  • d’Ettorre, P., Deisig, N., Sandoz, J.C. (2017). Decoding ants’ olfactory system sheds light on the evolution of social communication. Commentary. Proceedings of the National Academy of Sciences USA, 114(34), 8911-8913.
  • Kelomey, A. E., Paraiso, A., Sina, H., Legout, H., Garnery, L., Baba-Moussa, L. (2017). Genetic characterization of the honeybee ectoparasitic mite Varroa destructor from Benin (West Africa) using mitochondrial and microsatellite markers. Experimental and Applied Acarology, 72(1), 61-67.
  • Monceau, K., Tourat, A., Arca, M., Bonnard, O., Arnold, G., Thiery, D. (2017). Daily and seasonal extranidal behaviour variations in the invasive yellow-legged hornet, Vespa velutina. Journal of Insect Behavior, 30, 220-230.
  • Rortais, A., Arnold, G., Dorne, J.L., More, S.J., Sperandio, G., Streissl, F., Szentes, C., Verdonck, F. (2017). Risk assessment of pesticides and other stressors in bees: principles, data gaps and perspectives from the European Food Safety Authority. Science of the Total Environment, 587-588, 524-537.
  • Rousset, M., Collet, C., Cens, T., Bastin, F., Raymond-Delpech, V., Massou, I., Menard, C., Thibaud, J.B., Charreton, M., Vignes, M., Chahine, M., Sandoz, J.C., Charnet, P. (2017). Honeybee locomotion is impaired by Am-CaV3 low voltage-activated Ca2+ channel antagonist. Scientific Reports, 7:41782, 1-10.
  • Techer, M.A., Clémencet J., Simiand C., Turpin P., Garnery L., Reynaud, B., Delatte, H. (2017) Genetic diversity and differentiation among insular honey bee populations in the southwest Indian Ocean likely reflect old geographical isolation and modern introductions. PLoS ONE 12(12): e0189234.


  • Carcaud, J., Giurfa, M., Sandoz J.C. (2016). Parallel olfactory processing in the honey bee brain: odor learning and generalization under selective lesion of a projection neuron tract. Frontiers in Integrative Neuroscience, 9: 75, 1-13.
  • Couto, A., Lapeyre, B., Thiéry, D., Sandoz, J.C. (2016). The olfactory pathway of the hornet Vespa velutina: new insights into the evolution of the hymenopteran antennal lobe. Journal of Comparative Neurology, 11: 2335-2359.
  • Miguel, I., Garnery, L., Iriondo, M., Baylac, M., Manzano, C., Sheppard, W.S., Estonba, A. (2016). Origin, evolution and conservation of the honey bees from La Palma Island (Canary Islands): molecular and morphological data. Journal of Apicultural Research, 54(5), 427-440.


  • Achou, M., Loucif-Ayad, W., Legout, H., Hmidan, H., Alburaki, M., Garnery, L. (2015). An Insightful Molecular Analysis Reveals Foreign Honeybees Among Algerian Honeybee Populations (Apis mellifera L.). J Data Mining Genomics Proteomics, 6(166), 2153-0602.
  • Arca, M., Mougel, F., Guillemaud, T., Dupas, S., Rome, Q., Perrard, A., Muller, F., Fossoud, A., Capdevielle-Dulac, C., Torres-Leguizamon, M., Chen, X.X., Tan, J.L., Jung, C., Villemant, C., Arnold, G. and Silvain, J.F. (2015). Reconstructing the invasion and the demographic history of the yellow-legged hornet, Vespa velutina, in Europe. Biological Invasions, 17(8), 2357-2371.
  • Bertrand, B., Alburaki, M., Legout, H., Moulin, S., Mougel, F., Garnery, L. (2015). MtDNA COI‐COII marker and drone congregation area: An efficient method to establish and monitor honeybee (Apis mellifera L.) conservation centres. Molecular Ecology Resources, 15(3), 673-683.
  • Carcaud, J., Giurfa, M., Sandoz J.C. (2015). Differential combinatorial coding of pheromones in two olfactory subsystems of the honeybee brain. Journal of Neuroscience, 35, 4157-4167.
  • Charreton, M., Decourtye, A., Henry, M., Rodet, G., Sandoz, J.C., Charnet, P., Collet, C. (2015). A locomotor deficit induced by sublethal doses of pyrethroid and neonicotinoid insecticides in the honeybee Apis mellifera. PLoS ONE, 10(12): e0144879, 1-14.
  • Cholé, H., Junca, P., Sandoz, J.C. (2015). Appetitive but not aversive olfactory conditioning modifies antennal movements in honey bees. Learning and Memory, 22, 604-616.
  • Cens, T., Rousset, M., Collet, C., Charreton, M., Garnery, L., Le Conte, Y., Chahine, M., Sandoz, J.C., Charnet, P. (2015). Molecular characterization and functional expression of the voltage dependent Ca2+ channels from the honeybee Apis mellifera. Insect Biochemistry and Molecular Biology, 58, 12-27.
  • Devaud, J.M., Papouin, T. Carcaud, J., Sandoz, J.C., Grünewald, B., Giurfa, M. (2015). A neural substrate for higher-order learning in an insect: mushroom bodies are necessary for configural discriminations. Proceedings of the National Academy of Sciences USA, 112 (43), E5854–E5862.
  • Junca, P., Sandoz, J.C. (2015). Heat perception and aversive learning in honey bees: putative involvement of the thermal/chemical sensor AmHsTRPA. Frontiers in Physiology, 6: 316, 1-15.
  • Loucif-Ayad, W., Achou, M., Legout, H., Alburaki, M., Garnery, L. (2015) Genetic assessment of Algerian honeybee populations by microsatellite markers Apidologie 46:392-402.
  • Roselino, A.C., Hrncir, M., da Cruz Landim, C., Giurfa, M., Sandoz, J.C. (2015). Sexual dimorphism and phenotypic plasticity in the antennal lobe of a stingless bee Melipona scutellaris. Journal of Comparative Neurology, 523, 1461-1473.
  • Schubert, M., Sandoz, J.C., Galizia, C.G., Giurfa, M. (2015). Odorant dominance in olfactory mixture processing: what makes a strong odorant? Proceedings of the Royal Society B, 282 (1802), 1-10


  • Arca, M., Papachristoforou, A., Mougel, F., Rortais, A., Monceau, K., Bonnard, O., Tardy, P., Thiéry, D., Silvain, J.F., Arnold, G. (2014). Defensive behaviour of Apis mellifera against Vespa velutina in France: testing whether European honeybees can develop an effective collective defence against a new predator. Behavioural Processes, 106, 122-129.
  • Brandstaetter, A.S., Bastin, F., Sandoz, J.C. (2014). Honeybee drones are attracted by groups of consexuals in a walking simulator. Journal of Experimental Biology, 217, 1278-1285.
  • Couto, A., Monceau, K., Bonnard, O., Thiéry, D., Sandoz, J.C. (2014). Olfactory attraction of the hornet Vespa velutina to honeybee colony odors and pheromones. PLoS ONE, 9(12), e115943, 1-19.
  • Junca, P., Carcaud, J., Moulin, S., Garnery, L., Sandoz, J.C. (2014). Genotypic influence on aversive conditioning in honeybees, using a novel thermal reinforcement procedure. PLoS ONE, 9(5), e97333, 1-13.
  • Matsumoto, Y., Sandoz, J.C., Devaud, J.M., Lormant, F., Mizunami, M., Giurfa, M. (2014). Cyclic nucleotide–gated channels, calmodulin, adenylyl cyclase and calcium/calmodulin-dependent protein kinase II are required for late but not early long-term memory formation in the honey bee. Learning and Memory, 20, 29-33.
  • Maxim, L., Arnold, G. (2014) Pesticides and bees: the need for a new regulatory framework. EMBO Reports, 15 (1), 4.
  • Mougel F., Poursat M.A., Beaume N., Vautrin D., Solignac M. (2014) High-resolution linkage map for two honeybee chromosomes: the hotspot quest. Molecular Genetics and Genomics, 289 (1), 11 – 24
  • Pinto, M. A., Henriques, D., Chávez-Galarza, J., Kryger, P., Garnery, L., Zee, R.V.D., … & Johnston, J. S. (2014). Genetic integrity of the Dark European honey bee (Apis mellifera mellifera) from protected populations: a genome-wide assessment using SNPs and mtDNA sequence data. Journal of Apicultural Research 53(2), 269-278.
  • Roussel, E., Carcaud, J., Combe, M., Giurfa, M., Sandoz, J.C. (2014). Olfactory coding in the honeybee lateral horn. Current Biology, 24, 561-567.


  • Alburaki, M., Bertrand, B., Legout, H., Moulin, S., Alburaki, A., Sheppard, W.S., Garnery, L. (2013). A fifth major genetic group among honeybees revealed in Syria  BMC Genetics, 14:117
  • Fontbonne, R., Garnery, L., Vidau, C., Aufauvre, J., Texier, C., Tchamitchian, S., El Alaoui, H., Brunet, J.L., Delbac, F., Biron, D.G. (2013). Comparative susceptibility of three Western honeybee taxa to the microsporidian parasite Nosema ceranae. Infection Genetics and Evolution, 17, 188-194.
  • Hatjina, F., Papaefthimiou, C., Charistos, L., Dogaroglu, T., Bouga, M., Emmanouil, C., Arnold, G. (2013). Sublethal doses of imidacloprid decreased size of hypopharyngeal glands and respiratory rhythm of honeybees in vivo. Apidologie , 44, 467-480.
  • Lefer, D., Perisse, E., Hourcade, B., Sandoz, J.C. , Devaud, J.M. (2013). Two waves of transcription are required for long-term memory in the honeybee. Learning and Memory, 20, 29-33.
  • Monceau, K., Arca, M., Leprêtre, L., Mougel, F., Bonnard, O., Silvain, J.F., Maher, N., Arnold, G., Thiéry, D. (2013). Native prey and invasive predator patterns of foraging activity: The case of the Yellow-Legged Hornet predation at European Honeybee hives. PLoS ONE , 8(6), e66492, 1-9.
  • Mota, T., Gronenberg, W., Giurfa, M., Sandoz, J.C. (2013). Chromatic processing in the anterior optic tubercle of the honeybee brain. Journal of Neuroscience, 33, 4-16.
  • Papachristoforou A., Rortais A., Bouga M., Arnold G., Garnery L. (2013). Genetic characterization of the Cyprian honey bee (Apis mellifera cypria) based on microsatellites and mitochondrial DNA polymorphisms. Journal of Apicultural Science, 57 (2), 127-134.


  • Arca, M., Capdevielle-Dulac, C., Villemant, C., Mougel, F., Arnold, G., Silvain, J.F. (2012). Development of microsatellite markers for the yellow-legged Asian hornet, Vespa velutina, a major threat for European bees. Conservation Genetic Resources, 4(2), 283-286.
  • Arenas, A., Giurfa, M., Sandoz, J.C., Hourcade, B., Devaud, J.M., Farina, W.M. (2012). Early olfactory experience induces structural changes in the primary olfactory centre of an insect brain. European Journal of Neuroscience, 35(5), 682-690.
  • Bessoltane, N., Toffano-Nioche, C., Solignac M., Mougel F. (2012). Fine scale analysis of crossover and non-crossover and detection of recombination sequence motifs in the honeybee (Apis mellifera). PLoS ONE, 7(5), e36229, 1-10.
  • Carcaud, J., Hill, T., Giurfa, M., Sandoz J.C. (2012). Differential coding by two olfactory subsystems in the honey bee brain. Journal of Neurophysiology, 108, 1106-1121.
  • Deisig, N., Kropf, J., Vitecek, S., Pevergne, D., Rouyar, A., Sandoz, J.C., Lucas, P., Gadenne, C., Anton, S., Barrozo, R. (2012). Differential interactions of sex pheromone and plant odour in the olfactory pathway of a male moth. PLoS ONE, 7(3), e33159, 1-10.
  • Galizia, C.G., Franke, T., Menzel, R., Sandoz, J.C. (2012). Optical imaging of concealed brain activity using a gold mirror in honeybees. Journal of Insect Physiology , 58(5), 743-749.
  • Giurfa, M., Sandoz, J.C. (2012). Invertebrate learning and memory: fifty years of olfactory conditioning of the proboscis extension response in honey bees. Learning and Memory, 19, 54-66.
  • Matsumoto, Y., Menzel, R., Sandoz, J.C., Giurfa, M. (2012). Revisiting olfactory classical conditioning of the proboscis extension response in honey bees: a step toward standardized procedures. Journal of Neuroscience Methods, 211(1), 159-167.
  • Mougel, F., Solignac, M., Vautrin, D., Baudry, E., Ogden, J., Tchapla, A., Schweitz, H., Gilbert, H.(2012). Quantitative traits loci (QTL) involved in body colour, wing morphometry, cuticular hydrocarbons and venom components in honeybee. Apidologie, 43(2), 162-181.
  • Papachristoforou, A., Kagiava, A., Papaefthimiou, C., Termentzi, A., Fokialakis, N., Skaltsounis, A.L., Watkins, M., Arnold,G., Theophilidis,G. (2012). The bite of the honeybee: 2-heptanone secreted from honeybee mandibles during a bite acts as a local anaesthetic in insects and mammals. PLoS ONE, 7(10): e47432, 1-11.

Institutional reports

  • Arnold, G. (2017). Co-author of the report from the European Food Safety Agency (EFSA): Specifications for field data collection contributing to honey bee model corroboration and verification. EFSA Supporting publication, DOI: 10.2903/sp.efsa.2017.EN-1234
  • Arnold, G. (2016). Co-author of the report from the European Food Safety Agency (EFSA): Assessing the health status of managed honeybee colonies (HEALTHY-B): a toolbox to facilitate harmonised data collection. EFSA Journal,14(10):4578. DOI: 10.2903/j.efsa.2016.4578. http://onlinelibrary.wiley.com/doi/10.2903/j.efsa.2016.4578/epdf
  • Arnold, G. (2016). Co-author of the report from the European Food Safety Agency (EFSA): A mechanistic model to assess risks to honeybee colonies from exposure to pesticides under different scenarios of combined stressors and factors. EFSA Supporting publication, 13:7. DOI: 10.2903/sp.efsa.2016.EN-1069. http://onlinelibrary.wiley.com/doi/10.2903/sp.efsa.2016.EN-1069/pdf
  • Arnold, G. (2015). Co-author of the report from the French Food, Environment and Work Safety Agency (Anses): Co-exposition des abeilles aux facteurs de stress. https://www.anses.fr/fr/system/files/SANT2012sa0176Ra.pdf
  • Arnold, G.(2014). Expert for the report from the European Food Safety Agency (EFSA): Towards an integrated environmental risk assessment of multiple stressors on bees: review of research projects in Europe, knowledge gaps and recommendations’. EFSA Journal, 12(3):3594. DOI:10.2903/j.efsa.2014.3594.http://www.efsa.europa.eu/en/efsajournal/doc/3594.pdf
  • Arnold, G. (2013). Co-author of the report from the European Food Safety Agency (EFSA): Guidance Document on the risk assessment of plant protection products on bees (Apis mellifera, Bombus spp. and solitary bees). EFSA Journal,11(7): 3295. DOI:10.2903/j.efsa.2013.3295.http://www.efsa.europa.eu/en/efsajournal/doc/3295.pdf
  • Arnold, G. (2012). Co-author of the report from the European Food Safety Agency (EFSA): Scientific Opinion on the science behind the development of a risk assessment of Plant Protection Products on bees (Apis mellifera, Bombus spp. and solitary bees). EFSA Journal, 10(5): 2668. DOI:10.2903/j.efsa.2012.2668.http://www.efsa.europa.eu/en/efsajournal/doc/2668.pdf

National journal article

  • Arnold G. (2016). La santé environnementale. Le point de vue de l’expert public. Revue Experts, 126, 88-90.
  • Maxim L., Arnold G. (2015). Les chercheurs au cœur de l’expertise. Hermès, 73, 168-169.
  • Maxim L., Arnold G. (2012). Entre recherche académique et expertise scientifique : des mondes de chercheurs. Hermès, 64, 9-13.
  • Maxim L., Arnold G. (2012). Comment les conflits d’intérêts peuvent influencer la recherche et l’expertise. Hermès, 64, 48-59.

Book Chapters

  • Eouzan, I., Garnery, L., Sime-Ngando, T., Biron, DG. (2017). Les pesticides, la cause du déclin de l’abeille domestique ? In: Ecotoxicologie des communautés et impacts sur les fonctions des écosystèmes. Eds Bernard C, Mougin C, Pery A, ISTE Editions, Paris.
  • Sandoz, J.C. (2013). Neural correlates of olfactory learning in the primary olfactory center of the honeybee brain: the antennal lobe. In: Invertebrate Learning and Memory, Menzel, R. and Benjamin. P.R. Eds. Elsevier, San Diego (USA), 12 pp.