Research aims

Sensory systems are at the interface between an animal’s environment and its physiology and behavior. They determine how animals perceive the world, and respond to it through their behavior. Consequently, our working hypothesis is that the evolution of sensory systems plays a central role in the adaptation of behavior to environmental change or the occupation of new ecological niches. By combining new methods in genomics, genetics and neuroethology, we will explore different facets of the evolution of sensory systems, in particular chemosensory systems, and their involvement in a major transition in the organization of living organisms, i.e. the appearance of the highest degree of social life (eusociality). Our study models will mainly be hymenopteran insects, an order known to have undergone at least 9 emergences independent of eusociality. We will work on both social Hymenoptera (honey bees, bumblebees, vespid wasps and ants) and solitary ones (parasitic wasps, solitary bees, etc.).

1. Functional analysis of chemosensory systems:

Analysis of the evolution of chemosensory systems in Hymenoptera is hampered by our still limited knowledge of the function of the different chemosensory receptor families (encoded by genes belonging to the OR, IR and GR families), i.e. the odorant molecules detected by these receptors. Social insects, such as honeybees, use a plethora of pheromonal compounds to communicate within the colony (alarm, aggregation, queen fertility, brood condition, foraging stimulation, etc.). In order to link the different families of receptors to their function and role in social life, we are developing our heterologous expression approaches for genes encoding chemoreceptors (mainly OR genes). Using the honey bee as a model, we are studying adaptations in the processing of social olfactory information, using a range of behavioral, neuroanatomical and functional approaches (electrophysiological recordings of the antennal senses or in vivo imaging of nerve activity in the brain). We also use transgenic approaches to confirm the function of the genes encoding the chemoreceptors studied, and to create new neurogenetic tools in our model species, Apis mellifera.

2. Plasticity of chemosensory systems:

As insect sensory adaptation also involves plasticity over the life course, some of our projects are developed at the interface with ecology and experimental psychology. On the one hand, we are examining changes in chemosensory systems in heterogeneous and/or changing environments. On the other hand, since learning and memory represent a crucial form of this plasticity throughout life, we are also studying the role of learning in the adaptation of the chemosensory system. In the context of our questions on the multiple impacts of global change, we are seeking to understand how stresses, such as the presence of pesticides or temperature variations, influence the functioning of chemosensory systems and the learning and memory capacities of insects.

3. Evolution of sensory systems and the brain:

We are studying the evolutionary dynamics of the gene families encoding chemosensory receptors in insects, seeking to identify the specific dynamics existing in Hymenoptera, in relation to ecological and behavioral parameters, in particular linked to eusociality. In parallel, using neuroanatomical approaches, we are linking the evolution of brain structures in Hymenoptera to evolutionary trade-offs between olfactory and visual systems, and to the complexity of the olfactory system (structure and number of functional units within the primary olfactory center, the antennal lobe, or the higher integration centers, the mushroom bodies).

Members

Researchers and Lecturers

  • Jean-Christophe Sandoz, CNRS Research Director, Group 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).
  • Julie Carcaud, Assistant Professor, Paris-Saclay University. Evolution of gustatory and olfactory systems in bees: behavioural and neurophysiological approaches.
  • Line Duportets, Assistant Professor, Université Paris-Saclay. Reproductive physiology and behavior in honey bees.
  • 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.
  • Didier Casane, Professor Université Paris Cité.

Engineers et Technicians

  • Gaëlle Claisse, CNRS Engineer. Genome Editing and olfaction in honey bees.
  • Virginie Larcher, CNRS Assistant Engineer. Neuroanatomy and neurophysiology in Hymenoptera.

Postdocs

  • Julia Mariette, Postdoc. Coding of pheromonal information in the honey bee brain
  • Lohan Valadares, Postdoc. Biogenic amines and dominance hierarchies in ants

PhD students

  • Benjamin Andreu, PhD Student. Neural representation of social pheromones in honeybees.
  • Loïc Colin, PhD Student. Effects of pesticides on learning and memory in honey bees.
  • Simon Marty, PhD Student. Evolution of the olfactory system in Hymenoptera.
  • Melissa Pitzalis, PhD student. Gustatory coding in the honeybee brain.

Master students

  • Alizée Delarue, Master Student. Functional study of pheromone receptors in honey bees
  • Lucie Savignac, Master Student. Neuroanatomical study of the olfactory pathway of jewel wasps.

 

Alumni

  • Mariangela Arca, PhD student. Genetic characterization and behavioural study of an invasive hornet species in France: Vespa velutina.
  • Aurore Avarguès-Weber, Post-PhD student. Non-elementary learnings on compensator of locomotion
  • Florian Bastin, PhD student. Evolution of sexual communication in the bee.
  • Andreas Brandstaetter, NeRF Postdoctoral fellow. Evolution of pheromonal communication in the genus Apis.
  • Hanna Cholé, PhD Student. Social learning in honeybees.
  • Antoine Couto, PhD student, then postdoc. Behaviour and neuroanatomy of the invasive hornet Vespa velutina.
  • Nicholas Henderson, Master 2 Research student. Olfactory mixture learning in honeybees.
  • Kevin Fradin. 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.
  • Thierry Louis, Postdoc. Study of honeybee olfactory receptors.
  • Amélie Noël, CNRS Assistant Engineer (on contract). IDEX Paris-Saclay.
  • Ana-Carolina Roselino, FAPESP postdoctoral fellow. Neuroanatomy of the stingless bee brain.
  • Marie-Anne Wycke, Master 2 Research student. Learning of olfactory mixtures in honeybees.

Team Publications

2024

  • Policarpo M., Legendre L., Germon I., Lafargeas P., Espinasa L., Rétaux S. and Casane D. (2024) The nature and distribution of non-functional alleles suggest only two independent events at the origins of Astyanax mexicanus cavefish populations. BMC Ecology and Evolution in press
  • Policarpo M., Baldwin M., Casane D. and Salzburger W. (2024) Diversity and evolution of the vertebrate chemoreceptor gene repertoire. Nature communications 15:1421
  • Bastide H, Legout H, Dogbo N, Ogereau D, Prediger C, Carcaud J, Filée J, Garnery L, Gilbert C, Marion-Poll F, Requier F, Sandoz JC & Yassin A (2024) The genome of the blind bee louse fly reveals deep convergences with its social host and illuminates Drosophila origins. Current Biology, https://doi.org/10.1016/j.cub.2024.01.034 

 

2023

  • Valadares, L., Bueno da Silva, I., Costa-Leonardo, A.M., Sandoz, J.C. (2023). Differentiation of workers into soldiers is associated with a size reduction of higher-order brain centers in the neotropical termite Procornitermes araujoi. Scientific Reports, 13 (1), 18279, 1-11.
  • Couto, A., Marty, S., Dawson, E.H., d’Ettorre, P., Sandoz, J.C.*, Montgomery, S.H.* (2023). Evolution of the neuronal substrate for kin recognition in social Hymenoptera. Biological Reviews, 98, 2226–2242.
  • Rodríguez-Machado S., Ponce de León J.L., Germon I., Casane D. and García-Machado E. (2023) Phylogeography of Limia vittata (Cyprinodontiformes: Poeciliidae): geographical distribution of mitochondrial haplotypes is comparable to other Cuban poeciliids. Biological Journal of the Linnean Society 140(3): 459-470
  • Carcaud, J., Sandoz, J.C. (2023). Insect Neuroethology: more than behavior and neurons. Current Opinion in Insect Science, 57, 101037, 1-3.
  • Mariette, J., Noël, A., Louis, T., Montagné, N., Chertemps, T., Jacquin-Joly, E., Marion-Poll, F., Sandoz, J.C. (2023). Transcuticular calcium imaging as a tool for the functional study of insect odorant receptors. Frontiers in Molecular Neuroscience, 16, 1182361, 1-14.
  • Hyacinthe C., Attia J., Schutz E., Lego L., Casane D. and Rétaux S. (2023) Acoustic signatures in Mexican cavefish populations inhabiting different caves. PLoS ONE 18(8):e0289574
  • Carcaud, J., Otte, M., Grünewald, B., Haase, A.*, Sandoz, J.C.*, Beye, M.* (2023). Multisite imaging of neural activity using a genetically encoded calcium sensor in the honey bee. PLoS Biology, 21(1), e3001984, 1-20.
  • Legendre L., Rode J., Germon I., Pavie M., Quiviger C., Policarpo M., Leclercq J., Pere S., Fumey J., Hyacinthe C., Ornelas-Garcia P., Espinasa L., Retaux S. and Casane D. (2023) Genetic identification and reiterated captures suggests that the Astyanax mexicanus El Pachon cavefish population is closed and declining. Zoological Research 44(4): 701-711
  • Piqueret, B., Montaudon, E., Devienne, P., Leroy, C., Marangoni, E., Sandoz, J.C.*, d’Ettorre, P.* (2023). Ants act as olfactory bio-detectors of tumours in patient-derived xenograft mice. Proceedings of the Royal Society B, 290 (1991), 20221962, 1-8.
  • Syed A.S., Sharma K., Policarpo M., Ferrando S., Casane D. and Korsching S.I. (2023) Ancient and nonuniform loss of olfactory receptor expression renders the shark nose a de facto vomeronasal organ. Molecular Biology and Evolution 40(4):msad076
  • Piqueret, B., Sandoz, J.C., d’Ettorre, P. (2023). Disease detection using animal olfaction: the neglected potential of invertebrates. Frontiers in Ecology and Evolution, 10, 960757, 1-10.

 

2022

  • Bestea, L., Paoli, M., Arrufat, P., Carcaud, J., Sandoz, J.C., Velarde, R., Giurfa, M., de Brito Sanchez, M.G. (2022). The short neuropeptide F regulates appetitive but not aversive responsiveness in a social insect. iScience, 25(1), 103619, 1-22.
  • Policarpo M., Bemis K.E., Laurenti P., Legendre L., Sandoz J.C., Rétaux S. and Casane D. (2022) Coevolution of the olfactory organ and its receptor repertoire in ray-finned fishes. BMC Biology 20:195
  • Bestea, L., Briard, E., Carcaud, J., Sandoz, J.C., Velarde, R., Giurfa, M., de Brito Sanchez, M.G. (2022). Short neuropeptide F (sNPF) promotes the acquisition and formation of visual memories in honey bees. Biology Letters, 18, 20210520, 1-5.
  • Capela, N., Dupont, Y. L., Rortais, A., Sarmento, A., Papanikolaou, A., Topping, C. J., Arnold, G., . . . Sousa, J.P. (2022). High accuracy monitoring of honey bee colony development by a quantitative method. Journal of Apicultural Research, 1-10. doi:10.1080/00218839.2022.2098899.
  • Cholé, H., Merlin, A., Henderson, N., Paupy, E., Mahé, P., Arnold, G., Sandoz, J. C. (2022). Antenna movements as a function of odorants’ biological value in honeybees (Apis mellifera L.). Scientific Reports, 12, 11674, 1-16.
  • Coureaud, G., Thomas-Danguin, T., Sandoz, J.C., Wilson, D.A. (2022). Biological constraints on configural odour mixture perception. Journal of Experimental Biology, 225(6): jeb242274, 1-10.
  • Piqueret, B., Bourachot, B., Leroy, C., Devienne, P., Mechta-Grigoriou, F., d’Ettorre, P. *, Sandoz, J.C.* (2022). Ants detect cancer cells through volatile organic compounds. iScience, 25(3), 103959, 1-12.
  • Policarpo, M., Bemis, K.E., Laurenti, P., Legendre, L., Sandoz, J.C., Rétaux, S., Casane, D. (2022). Coevolution of the olfactory organ and its receptor repertoire in ray-finned fishes. BMC Biology, 20:195, 1-10.
  • Valadares, L., Vieira, B.G., Santos do Nascimento, F., Sandoz, J.C. (2022). Brain size and behavioral specialization in the jataí stingless bee (Tetragonisca angustula). Journal of Comparative Neurology, 530 (13), 2304-2314.

 

2021

  • Arnold, G. (2021). Conflicts of interest and improvement through peer review: the case of IPBES report on pollinators. Current Opinion in Insect Science, 46, 57–63.
  • Van Helden J., Butler C.D., Achaz G., Canard B., Casane D., Claverie J.-M., Colombo F., Courtier V., Ebright R.H., Graner F., Leitenberg M., Morand S., Petrovsky N., Segreto R., Decroly E., Halloy J. (2021) An appeal for an objective, open, and transparent scientific debate about the origin of SARS-CoV-2. The Lancet 398(10309):1402–1404
  • Bestea, L., Réjaud, A., Sandoz, J.C., Carcaud, J., Giurfa, M., de Brito Sanchez, M. G. (2021). Peripheral Taste Detection in Honey Bees: What do Taste Receptors Respond to? European Journal of Neuroscience (in press).
  • Policarpo M., Bemis K.E., Tyler J.C., Metcalfe C.J., Laurenti P., Sandoz J.C., Rétaux S. and Casane D. (2021) Evolutionary dynamics of the OR gene repertoire in teleost fishes: evidence of an association with changes in olfactory epithelium shape. Molecular Biology and Evolution 38(9):3742–3753
  • Couto, A., Arnold, G., Ai, H., Sandoz, J.C. (2021). Interspecific variation of antennal lobe composition among four hornet species. Scientific Reports, 11, 20883, 1-12.
  • Sallard E., Halloy J., Casane D., Decroly E., van Helden J. (2021) Tracing the origins of SARS-COV-2 in coronavirus phylogenies: a review. Environmental Chemistry Letters published online Feb 4:1–17
  • Mariette, J., Carcaud, J., Sandoz, J.C. (2021). The neuroethology of olfactory sex communication in the honeybee Apis mellifera. Cell and Tissue Research, 383, 177–194.
  • Policarpo M., Fumey J., Lafargeas P., Naquin D., Thermes C., Naville M., Dechaud C., Volff J.-N., Cabau C., Klopp C., Møller P.R., Bernatchez L., García-Machado E., Rétaux S. and Casane D. (2021) Contrasting gene decay in subterranean vertebrates: insights from cavefishes and fossorial mammals. Molecular Biology and Evolution 38(2):589–605
  • Mertes, M., Carcaud, J., Sandoz, J.C. (2021). Olfactory coding in the antennal lobe of the bumble bee Bombus terrestris. Scientific Reports, 11, 10947, 1-14.
  • Policarpo M., Bemis K.E., Tyler J.C., Metcalfe C.J., Laurenti P., Sandoz J.C., Rétaux S. and Casane D. (2021). Evolutionary dynamics of the OR gene repertoire in teleost fishes: evidence of an association with changes in olfactory epithelium shape. Molecular Biology and Evolution, 38(9), 3742-3753.

 

2020

  • Lai, Y., Despouy, E., Sandoz, J.C., Su, S., de Brito Sanchez, G., Giurfa, M. (2020). Degradation of an appetitive olfactory memory via devaluation of sugar reward is mediated by 5-HT 2 signaling in the honey bee. Neurobiology of Learning and Memory, 107278, 1-13.
  • Wycke, M.A. Coureaud, G., Thomas-Danguin, T., Sandoz, J.C. (2020). Configural perception of a binary olfactory mixture in honey bees as in humans, rodents and newborn rabbits. Journal of Experimental Biology 223, jeb22761, 1-12.
  • Hernández D., Møller P.R., Casane D. and García-Machado E. (2020) A new species of the cave-fish genus Lucifuga (Ophidiiformes, Bythitidae), from eastern Cuba. ZooKeys 946:17-35
  • García-Machado E., Ponce de Léon J.L., Gutiérrez-Costa M.A., Michel-Salzat A., Germon I. and Casane D. (2020) Phylogeographic evidence that the distribution of cryptic euryhaline species in the Cuban Gambusia punctata species group was shaped by the archipelago geological history. Molecular Phylogenetics and Evolution 144:106712
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2019

  • Cholé, H., Carcaud, J., Mazeau, H., Famié, S., Arnold, G., Sandoz, J.C. (2019). Social contact acts as appetitive reinforcement and supports associative learning in honeybees. Current Biology, 29(8), 1407-1413.
  • Junca, P., Garnery, L., Sandoz, J.C. (2019). Genotypic trade-off between appetitive and aversive capacities in honeybees. Scientific Reports (in press).
  • Piqueret, B., Sandoz, J.C., d’Ettorre, P. (2019). Ants learn fast and do not forget: olfactory associative learning and extinction in Formica fusca. Royal Society Open Science, 6: 190778, 1-11.
  • Yanagawa, A., Couto, A., Sandoz, J.C., Hata, T., Mitra, A., Ali Agha, M., Marion-Poll, F. (2019). LPS perception through a taste-induced reflex in Drosophila. Journal of Insect Physiology, 112, 39-47.

 

2018

  • Bastin, F., Couto, A. , Larcher, V., Phiancharoen, M., Koeniger, G., Koeniger, N., Sandoz, J.C. (2018). Marked inter-specific differences in the neuroanatomy of the male olfactory system of honey bees (genus Apis). Journal of Comparative Neurology, 526, 3020-3034.
  • 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, 526, 2068–2077.
  • 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, 155, 556-567.
  • 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.

Books

  • « Les Abeilles face au risque toxique », Editors: Charnet, P, Sandoz, J.C., Collet, C. (2022), CNRS Editions (450 p)

Book Chapters

  • Noël, A. & Sandoz, J.C. (2022) La colonie d’abeilles : un système complexe et fragile. In: Collet, C., Sandoz, J.C., Charnet, P. (eds). Les abeilles face au risque toxique. CNRS Editions, 43-64.
 
 
 
 
 
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