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Neural and Molecular Mechanisms Underlying the Olfactory Modulation of Aggression in Honeybees Morgane Valérie Martine Nouvian Bsc, Msc

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Neural and Molecular Mechanisms Underlying the Olfactory Modulation of Aggression in Honeybees Morgane Valérie Martine Nouvian Bsc, Msc Neural and molecular mechanisms underlying the olfactory modulation of aggression in honeybees Morgane Valérie Martine Nouvian BSc, MSc A thesis submitted for the joint degree of Doctor of Philosophy at The University of Queensland Queensland Brain Institute & Université Toulouse 3 Paul Sabatier Centre de Recherche sur la Cognition Animale ED BSB: Neurosciences And defended the 21st of September 2016 in front of the following jury: Pr. Alison Mercer (examiner) Pr. Yves Le Conte (examiner) Dr. Judith Reinhard (UQ thesis supervisor) Pr. Martin Giurfa (UPS thesis supervisor) Abstract Although honeybees were domesticated over 7000 years ago, finding ways to manage their defensive responses against intruders, including humans, is still a current challenge. This is in part due to the complexity of this behaviour, which starts with the detection of the threat by a few specialized individuals and culminates into a generalized, collective attack triggered by the release of an alarm pheromone. Numerous studies have investigated honeybee aggression and stinging behaviour both in the laboratory and field, including the sensory triggers and the potential regulatory mechanisms. However the specific neural and molecular mechanisms regulating this behaviour are still unknown. In my PhD thesis, I investigated the role of olfactory signals and brain biogenic amines in modulating aggression in honeybees, integrating behavioural, physiological, and pharmacological experiments. Using a novel assay to measure the stinging behaviour of individual bees under controlled conditions, I first explored whether a range of plant odours could modulate aggression, in particular by interacting with the alarm pheromone released by aroused bees. I identified two floral compounds, linalool and 2-phenylethanol, that block the recruitment elicited by the alarm pheromone. These odours do not prevent the bees from perceiving the alarm pheromone. Instead, this blocking effect appears to correlate with the appetitive value of these odours. This suggests that a complex sensory integration takes place when honeybees are faced with the decision of engaging or not into defensive tasks. Furthermore, a field test demonstrated that linalool could also be used to manage aggressive colonies, highlighting the practical application of these findings. To gain a better understanding of the neuronal mechanism underlying this effect of floral odours on honeybee aggression, I next investigated how these floral compounds affect the representation of the alarm pheromone in the primary olfactory center of the honeybee brain, the antennal lobe, using in vivo calcium-imaging to monitor the activity of neurons in this area. The antennal lobes are structured into functional units called glomeruli, and an odour identity and concentration is encoded within the pattern and intensity of activated glomeruli. We expected that the representation of the mixture of an appetitive floral odour with the alarm pheromone may not be linearly obtained from the representation of each compound, thus ii revealing the neuronal mechanisms at play during our previous aggression assays. However, analysis of the data suggests no such mechanism, which could be a clue that this processing is happening in higher brain centers. Finally, I investigated the role of brain biogenic amines in honeybee aggression. Biogenic amines are important neuromodulators and have been implicated in the regulation of the aggressive behavior of a number of species. However, their potential role in regulating the honeybee’s stinging behavior had not been investigated so far. My experiments showed that bees from aggressive colonies have higher serotonin levels in their central brain than bees from gentle colonies. In this region, bees exposed to the alarm pheromone during an aggression test also had more dopamine and serotonin than control bees. Serotonin levels were also higher in the optic lobes of aggressive bees, and in the subesophageal zone of bees responding to the alarm pheromone. Pharmacologically increasing serotonin and dopamine levels induced higher aggressiveness in bees, while decreasing them reduced aggressiveness. This confirms for the first time that serotonin and dopamine play a key role in regulating honeybee aggression. This thesis is the first integrated study of the molecular and neural mechanisms underlying aggressive behaviour in honeybees. Importantly, this body of work does not only increase our understanding of honeybee behaviour, it will also find application in the development of novel, olfactory-based methods to control honeybee aggression. iii Résumé Malgré leur domestication il y a plus de 7000 ans, gérer la réponse défensive des abeilles, en particulier contre l’Homme, reste un défi. Cet état de fait est dû en partie à la complexité de cette réponse, qui commence par la détection du danger par quelques individus spécialisés et culmine dans une attaque collective, déclenchée par une phéromone d’alarme. Le comportement agressif des abeilles a fait l’objet de nombreuses études à la fois en laboratoire et sur le terrain, qui ont permis d’identifier les éléments déclencheurs et régulateurs de ce comportement. Cependant les mécanismes neuronaux et moléculaires qui sous-tendent cette réponse agressive sont toujours inconnus. Durant ma thèse, j’ai étudié le rôle des signaux olfactifs et des amines biogènes dans la régulation de l’agressivité des abeilles, en intégrant des approches comportementales, physiologiques et moléculaires. En utilisant un nouveau test pour mesurer la réponse agressive d’abeilles individuelles en conditions contrôlées, j’ai pu déterminer si certaines odeurs de plantes modulent l’agressivité des abeilles, en particulier en interagissant avec la phéromone d’alarme. J’ai identifié deux composés floraux, le linalol et le 2- phenylethanol, qui bloquent la réponse agressive déclenchée par la phéromone d’alarme. Ces odeurs n’empêchent pas les abeilles de sentir la phéromone d’alarme, mais ont une valeur appétitive importante pour les abeilles. Ces résultats suggèrent qu’une intégration sensorielle complexe a lieu lorsque les abeilles décident de participer ou non à la defense de la colonie. De plus, un test de terrain a montré que le linalol peut aussi être utilisé pour diminuer l’agressivité d’une colonie entière, ouvrant la voie pour des applications pratiques. Afin de mieux comprendre les mécanismes neuronaux responsables de cette modulation par des odeurs florales, j’ai ensuite regardé comment ces odeurs affectent la représentation de la phéromone d’alarme dans le centre olfactif primaire du cerveau de l’abeille, le lobe antennaire. J’ai ainsi utilisé l’imagerie calcique in vivo pour visualiser l’activité des neurones de cette région. Les lobes antennaires sont structurés en unités fonctionnelles appelées glomérules, et l’identité d’une odeur est codée par le patron d’activation des glomérules. Notre hypothèse était que la représentation d’un mélange entre une odeur de plante appétitive et la phéromone d’alarme ne peut pas être obtenu linéairement à partir de la représentation de chaque composé, révélant ainsi les mécanismes neuronaux à l’origine de l’effet de iv ces odeurs florales. Cependant l’analyse des données n’a pas mis en évidence ce phénomène, ce qui suggère que l’intégration de la valeur appétitive des odeurs a lieu dans des centres supérieurs. Finalement, j’ai examiné le rôle des amines biogènes dans le comportement agressif de l’abeille. Les amines biogènes sont d’importants neuromodulateurs qui ont été impliqués dans le contrôle de l’agressivité de nombreuses espèces, mais leur rôle chez l’abeille n’avait pas été démontré. Les abeilles de colonies agressives ont plus de sérotonine dans leur cerveau central que celles provenant de colonies dociles. Dans cette région, les abeilles ayant été exposées à la phéromone d’alarme ont aussi plus de dopamine et de sérotonine. Les niveaux de sérotonine sont aussi plus élevés dans les lobes optiques des abeilles agressives, et dans la zone suboesophageal des abeilles qui répondent à la phéromone d’alarme. Enfin, augmenter artificiellement les niveaux de sérotonine ou de dopamine induit plus de réponses agressives de la part des abeilles, et les diminuer réduit cette réponse. Ceci confirme le rôle clé de ces molécules. Ces travaux représentent la première étude intégrée des mécanismes moléculaires et neuronaux qui sous-tendent le comportement agressif des abeilles. En plus d’augmenter nos connaissances sur la biologie de l’abeille, ils permettent d’envisager de nouvelles méthodes, basées sur l’utilisation d’odeurs florales, pour contrôler leur agressivité. v Declaration by author This thesis is composed of my original work, and contains no material previously published or written by another person except where due reference has been made in the text. I have clearly stated the contribution by others to jointly-authored works that I have included in my thesis. I have clearly stated the contribution of others to my thesis as a whole, including statistical assistance, survey design, data analysis, significant technical procedures, professional editorial advice, and any other original research work used or reported in my thesis. The content of my thesis is the result of work I have carried out since the commencement of my research higher degree candidature and does not include a substantial part of work that has been submitted to qualify for the award of any other degree or diploma in any university or other tertiary institution. I have clearly
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